Michael D. Greenfield

Ultrasonic mate calling in the lesser wax moth

ABSTRACT. The lesser wax moth, Achroia grisella (Fabricius) (Pyralidae: Galleriinae), uses an altrasonic communication system for mate calling The male produces a 100 kHz sound by striking its tegula with the forewing. This calling sound induces virgin females to orient toward males. Although the pheromone released from the males wing glands may stimulate kinesis in females, it does not elicit orientation. Female moths are attracted toward synthetic 40 and 72 kHz sounds which simulate the pulse length and repetition rate of the males calling signal.

Katydids and Bush-Crickets: Reproductive Behavior and Evolution of the Tettigoniidae

OUR APPRECIATION OF biological diversity owesmuch to the collective efforts of a special cadre of scientists who become thoroughly captivated by particular organisms, recognize those central issues that can be studied with greatest precision in their favorite species, andenthusiastically advertise theirÞndings to the biological community. The Canadian behavioral ecologist Darryl Gwynne is among this breed, and his efforts have put katydids (bush-crickets, should you reside outside the Western Hemisphere) on the behavioral ecology and evolutionmap. True, bymid 20 century, katydids (Tettigoniidae) had already acquired some status in the natural history of North America through their mating songs, especially the variable syllables sung by Pterophylla camellifolia (true katydid). In addition, entomologists were becoming aware of the importance of these songs in species recognition, sexual advertisement, and male rivalry. But it was Darryl GwynneOs studies of mating systems inNorthAmerican andAustralian tettigoniids over the past 20 years Ð which have taught us so much about the evolution of courtship behavior and how ecological factors may insuence the roles assumed by the sexes Ð that earned this family a central place in biology. These landmark studies, accompanied by concise reviewsof theevolution, anatomy,physiology, and ecology of tettigoniids, are now presented in an eminently readable book, “Katydids and bush-crickets: reproductive behavior and evolution of the Tettigoniidae” (D.T. Gwynne, 2001, Cornell Univ. Press, 317 pp.). In nine chapters, Gwynne introduces us to the global diversity of the Tettigoniidae and its phylogenetic relationships to other Orthoptera, describes the basic biology of this family, and then focuses on Þve topics in reproductive behavior: pairing of the sexes as facilitated by acoustic and vibratory signals, courtship feeding and the evolution of spermatophore attachments, sexual selection, risks incurred by the signaler and receiver, and sexual roles in courtship. The last topic is given special attention, as some tettigoniids are noteworthy for variation and reversals in sexual roles. Thus, we learn about ardent and aggressive females, coy and discriminating males who donate as much or more material investment to their offspring as their female partners do, and the circumstances under which the insects may revert to habits more beÞtting their gender.Gwynnewrites inapersonal style, almost chatty in places, but he does not treat these observations as mere natural history oddities. Rather, he makes exemplary use of “the exception probes the rule” tactic to test and reÞne our understanding of the relationships between the sexes in animal mating systems. “Katydids and bush-crickets: reproductive behavior and evolution of the Tettigoniidae” is not, nor did its author intend it to be, an encyclopedic coverage of these insects. Readers desiring in-depth treatment of speciÞc subjects including tettigoniid systematics, acoustic behavior, and neurobiology may be better served by consulting the (slightly out-of-date) edited volume “The Tettigoniidae: biology, systematics and evolution”(W.J.Bailey andD.C.F.Rentz, [eds.], 1990, Springer-Verlag, 395 pp.). Instead, Darryl GwynneOs recent book guides the reader through the complex interplay among ecology, evolution, and behavior that has shapedcourtship interactions,mating systems, and sexual differences. Sexual selection theory is clearly a prevailing theme, and its nuances are carefully explained so that one may evaluate the various hypotheses derived from its application. Such application is particularly well developed for analyzing the evolution of the tettigoniid spermatophore, which is accounted forbyno fewer than10potential explanations based largely on sexual selection. Importantly, the explanation thatemerges fromcurrentanalysis asmost likely in general (ejaculate protection) is not that which the author favored in his initial research (paternal investment). As indicated above, “Katydids and bush-crickets” is not a book about mechanisms. Given its stated focus, this is Þne, but there are several places in which I would have preferred a stronger physiological or genetic approach: biomechanical and neurophysiological factors, in addition to ecological ones, do constrain the sorts of songs that katydids can sing and hear, and genetic aspects of signaling, mating preferences, and changes leading to speciation deserve more attention. Similarly, could better understanding of development and nutritional biochemistry provide new insight to the katydid spermatophore? The book includes a number of valuable comparisons with other insects, but several critical ones were not made. For example, gregarization in the decticine katydidAnabrus simplex (Mormon Cricket) is discussed, but there is scant mention of the “locust phenomenon” in Old World Acrididae. Could information on factors regulating locust populations and their movement help explain how tettigoniid hordes periodically form and march across the Great Basin? These points notwithstanding, Darryl Gwynne has written a book that is both informative and provocative. He has combined his considerable literary panachewith extensive knowledge of tettigoniid biology anda sophisticatedunderstandingofevolution tooffer us an exciting view of a magniÞcent group of insects. Moreover, he demonstrates how tettigoniids have served as organisms par excellence for studying diverse aspects of courtship: acoustic communication, parental investment, sexual role reversals. The book is superbly illustrated with Þgures, line drawings, and colorplatesof tettigoniids fromthevariouscontinents.

Precedence effects and the evolution of chorusing

The structured choruses produced by rhythmically signalling males in many species of acoustic animals have long–captured the imagination of evolutionary biologists. Though various hypotheses have been forwarded to explain the adaptive significance of such chorusing, none have withstood empirical scrutiny. We suggest instead that alternating and synchronous choruses represent collective epiphenomena resulting from individual males competing to jam each others signals. These competitions originate in psychoacoustic precedence effects wherein females only orient toward the first call of a sequence, thus selectively favouring males who produce leading calls. Given this perceptual bias, our modelling confirms that a resetting of signal rhythm by neighbours’ signals, which generates either alternation or synchrony, is evolutionarily stable provided that resetting includes a relativity adjustment for the velocity of signal transmission and selective attention toward only a subset of signalling neighbours. Signalling strategies in chorusing insects and anurans are consistent with these predicted features.

Genotype–environment interaction and the reliability of mating signals

I t is a central tenet of animal communication theory that signals are reliable (Zahavi 1977). That is, the characteristics of a signal that are attended to by a receiver should be reasonably good predictors of the transmitter’s current physical ability, internal state or motivation, social status, or acquired information. Signal characteristics should also predict the future consequences that a receiver, responding in a particular way, is likely to experience. Whereas the range of signals that animals transmit between one another may certainly include some messages that are not fully honest (Hasson 1994; e.g. Backwell et al. 2000), and partially withholding information or identity can sometimes be in a transmitter’s best interest (Johnstone 1997), animal communications are generally expected to result in a net benefit to both signaller and receiver (see Hauser 1996; Bradbury & Vehrencamp 1998). This expectation rests on the reasoning that failure to meet the criterion of reliability, as when an ‘inferior’ individual broadcasts a ‘strong’ signal normally associated with superior physical prowess, should result in selection against receiver responses to the signal, which, in turn, would select against its continued transmission, without alteration, by the signaller. In terms of perfection, signal characteristics are expected to be reliable to the extent that an ‘ideal receiver’, one suffering no perceptual impairments, can respond in a manner that on average enhances its fitness (see Johnstone & Grafen 1993). Within the realm of sexual selection, animal mating signals are expected to indicate the signaller’s phenotype with some degree of reliability. Moreover, under the various coevolutionary mechanisms of sexual selection (wherein mate choice only yields indirect, genetic benefits), mating signals are also expected to indicate the signaller’s genotype and, more critically, the phenotype of offspring that the signaller would sire. This latter expectation is most apparent in those processes

GENETIC VARIANCE OF SEXUALLY SELECTED TRAITS IN WAXMOTHS: MAINTENANCE BY GENOTYPE X ENVIRONMENT INTERACTION

Abstract.— .–When traits experience directional selection, such as that imposed by sexual selection, their genetic variance is expected to diminish. Nonetheless, theory and findings from sexual selection predict and demonstrate that male traits favored by female choice retain substantial amounts of additive genetic variance. We explored this dilemma through an ecological genetic approach and focused on the potential contributions of genotype X environment interaction (GEI) to maintenance of additive genetic variance for male signal characters in the lesser waxmoth, Achroia grisella (Lepidoptera: Pyralidae). We artificially selected genetic variants for two male signal characters, signal rate (SR) and peak amplitude (PA), that influence female attraction and then examined the phenotypic plasticity of these variants (high‐ and low‐SR and high‐ and low‐PA lines) under a range of environmental conditions expected in natural populations.

The question of paternal investment in Lepidoptera: male-contributed proteins in Plodia interpunctella

In Plodia interpunctella, radioactive labelling techniques indicate that male-derived substances, transferred to the female during copulation, enter unfertilized eggs. These substances are proteinaceous and the cumulative amount of material entering the unfertilized eggs increases with time since mating. Following courtship, smaller males complete coupling with females at a lower frequency than larger males. Smaller males also transfer smaller (by weight) ejaculates than larger males. Ejaculate weight is about 4% of male body weight in P. interpunctella. However, neither fecundity nor the number of deposited eggs are a function of ejaculate weight. Consequently, ejaculate materials cannot be designated a form of paternal investment, despite the observed transfer to unfertilized eggs.

GENETIC VARIANCE AND PHENOTYPIC PLASTICITY IN A COMPONENT OF FEMALE MATE CHOICE IN AN ULTRASONIC MOTH

Abstract.— Female response to male advertisement signals in lesser waxmoths showed substantial genetic variation, phenotypic plasticity across rearing environments, and genotype‐by‐environment interactions resulting in crossing reaction norms. These results represent two previously underemphasized means by which genetic variation may be maintained in sexually selected traits: genetic variation in female response to male traits, and variation in the selection acting on both males and females. Genotype‐by‐environment interactions and reaction norms that cross indicate that divergent selection may act on male and female sexual traits if the level of environmental change is high. The processes that contribute to the maintenance of genetic variation may thus also contribute to population differentiation.

When are good genes good? Variable outcomes of female choice in wax moths

Female lesser wax moths (Achroia grisella) choose males based on characters of their ultrasonic advertisement signals. Because a females opportunity to obtain increased somatic benefits by mating with a particular male is limited, we investigated whether females obtain genetic benefits for their offspring via mate choice. Controlled breeding experiments conducted under favourable food and temperature conditions showed that developmental characters are heritable, that sire attractiveness and offspring survivorship are unrelated, but that females mating with attractive signallers produce offspring who mature faster than the offspring of females mating with non–attractive signallers. However, under some unfavourable food or temperature conditions, it is the offspring of females mating with non–attractive males who mature faster; these offspring are heavier as well. Thus, the relationship between male attractiveness and offspring development is not environmentally robust, and support for a good genes model of mate choice in A. grisella is dependent on conditions. These findings suggest genotype–environment interactions and emphasize the necessity of testing sexual selection models under a range of natural environments.

Interspecific acoustic interactions among katydids Neoconocephalus: inhibition-induced shifts in diel periodicity

Abstract Males of the katydid Neoconocephalus spiza stridulate in a loud, chirping manner, but they are inhibited from singing during the uninterrupted songs of three sympatric congeners. Playback experiments using natural and synthetic stimuli showed that inhibition can be caused by any continuous or rapidly pulsing sound presented at an intensity greater than 40 dB sound pressure level and from 8 to 16 kHz in frequency, the approximate spectral range of the N. spiza chirps and the continuous songs of the congeneric species. In specific habitats where inhibiting species are absent, N. spiza sings primarily at night, but diurnal singing prevails where the inhibitors, all nocturnal, are found. Removal of the inhibiting species in a field experiment resulted in a rapid shift of the periodicity of N. spiza signalling from diurnal to nocturnal. This is the first reported case of a reversal in diel periodicity of singing caused by signal interference. It is argued that in a noisy environment, long-term temporal adjustments may be the most effective means of avoiding the problem of acoustic interference.

Absolute versus relative measurements of sexual selection:Assessing the contributions of ultrasonic signal characters to mate attraction in lesser wax moths, Achroia grisella (Lepidoptera:Pyralidae).

When females choose a mate among a group of signaling males concentrated in a small area, a males mating success is often determined not only by his absolute attractiveness but by the attractiveness of his neighbors as well. Multivariate analyses of sexual selection measurements based on absolute values of predictor variables are then misleading, because such analyses assume that the fitness of a given individual is not influenced by others. We addressed this problem of relative fitness in sexual selection by developing two adjustments of the predictor variables in the multivariate analyses by including group means in addition to absolute values and by using relative values, deviations from group means.