ABSTRACT

The three orders of Neuropterida are together considered to be the basal, most plesiomorphic representatives of the Endopterygota (= Holometabola; insects with complete metamorphosis). Therefore, their mating systems are particularly interesting from a phylogenetic perspective, in that they could provide insight into the ancient past of insect behavioral evolution. However, sexual behavior is extremely diverse within the 21 families of Neuropterida, and not unlike that found in insects that are usually considered more ‘advanced’. This chapter describes what little is known of sexual attraction, courtship and mating in the orders Megaloptera, Raphidioptera and Neuroptera. Each neurop – terid mating system shows clear signs of having been molded by the same intense and conflicting pressures of mate attraction and intersexual and intrasexual competition that have been described for other animal and plant groups. In the most plesiomorphic taxa (Sialidae, Raphidioptera, Ithonoidea), female pheromones serve to attract multiple males; this attraction has produced synchronized swarming behavior and male scramble–competition polygyny in some species. Also plesiomorphic and nearly universal within the superorder is sperm transfer by means of a large spermatophore, which can represent a significant paternal investment. Probably as a consequence, prolonged copulation and mate–guarding have evolved wherever particularly large spermatophores are exchanged. Courtship is found in the majority of Neuropterida, and is usually mediated by sex pheromones deployed by males from an anatomically diverse array of androconia (scent glands).

Sexual behavior and social behavior are profoundly alike in that both involve one set of individuals more or less willingly providing a limiting resource to another set (Queller 1994). Thus, in sexual interactions females provide resource–rich ova and other parental investment to males, and in social interactions workers provide labor to queens. In both situations, the parties are virtually always in conflict over the allocation of the resources, but their interests also partly coincide: eggs must be fertilized and offspring produced, and a new generation of reproductives must be successfully protected and reared. The complex mixtures of conflict and cooperation that thus typify sex and sociality make them among the most endlessly fascinating and difficult topics in ecology and evolution.

This book, and its companion (Choe and Crespi 1997), explore the intricacies of sexual and social competition. We have drawn together, for each of these topics, a set of authors whose expertise is both taxon–deep and broadly based in the theory that guides interpretation of natural history. Our goal has been to bring theory and observation together, to find parallels and convergences between disparate taxa, and to sketch out the patterns of engagement that will allow us to understand how conflicts and confluences of interest evolve together.

ABSTRACT

The male–female interaction is an asymmetrical, usually obligate mutualism in which there are conflicts of interest whenever multiple potential partners that vary in quality are available for either sex. Understanding male–female confluences and conflicts of interest is required to explain the sexual sequence and how it evolves. Mating interactions involve multiple steps or stages, distinguishable because of differences arising out of changes in selection that occur during the sequence. Sexual selection and competition take several different forms, which must be understood before accurate interpretations can be made of mating events in any particular case.

Sexual selection guided primarily by male–female conflicts of interest can result in resolvable evolutionary chases that lead to evolutionary stable strategies but perhaps more frequently lead to chases that tend to be unending (Parker 1979).

ABSTRACT

Pseudoscorpions are an ancient order of arachnids whose mating systems display an interesting mix of phylogenetic conservatism and evolutionary plasticity. A 400 millionyear– old pattern of indirect sperm transfer by means of spermatophores deposited on the substrate pervades all aspects of sexual selection in pseudoscorpions. Across families, mating behavior ranges from the ancestral condition, in which males deposit structurally simple spermatophores irrespective of the presence of females (non–pairing), to a derived condition in which males engage in elaborate courtship and assist females in the uptake of structurally complex spermatophores. In non–pairing taxa, sexual selection appears to be mediated through rapid male development and prolific spermatophore production. Males are invariably the smaller sex and do not fight over access to females. Why non–pairing has persisted in six of seven superfamilies remains an enigma. Cladistic analysis suggests that pair formation has evolved independently only once. Evidence from within the most diverse family, the Chernetidae, indicates that, once pair formation evolved, sexual dimorphism became a highly variable condition. Only in productive, and hence often ephemeral and patchily distributed, micro – habitats do populations reach densities at which selection for fighting ability outweighs the costs of attaining competitive size. The harlequin–beetle–riding pseudoscorpion, Cordylochernes scorpioides, has provided a model system both for assessing the influence of ecological factors on the operation of sexual selection and for identifying processes that can maintain variability in male sexually selected traits.

ABSTRACT

The mating signals and ecology of fireflies are diverse and the biology of exceptional species can be a source of historical information. Such species are functioning theoretical models and as working surrogates can be used for observational and experimental studies on the selection pressures, population divergences, and trajectories of history. Transitions between signaling modes and ecology, the impact of signal–focusing predators, and the influence of a species' unique ecology on its sexual biology are among phenomena that extant fireflies may illuminate. This paper describes idiosyncratic elements in the mating biology of several lampyrids, and then outlines some basic patterns in the mating biology of Photuris fireflies, themselves firefly predators and important agents of selection for many other fireflies.

INTRODUCTION

Fireflies initially caught my interest because they provided an opportunity to work taxonomically with a little–known group of attractive organisms, in the fashion of naturalists and curators of the past. Early observations by F. A. McDermott and H. S. Barber (1910–1951; review in Lloyd 1990) showed possibilities that existed. The renewed discussion of Darwin's sexual selection (Campbell 1972; Otte 1979), with the fresh perspectives for firefly systematics that were revealed (Lloyd 1979) and the Byzantine signal complexities and confusion of the genus Photuris and their interactions with species that occur with them, have sustained pursuit (Barber and McDermott 1951; McDermott 1967; Lloyd 1969a, 1980,1981a,b, 1984a,b, 1986, J. E. Lloyd, taxonomic monograph in preparation).

ABSTRACT

Sexual selection in resource defense polygyny systems is characterized by male–male competition for valuable resource patches, female settlement among patches based on both resource quality and male quality, and positive correlations between resource quality and male quality. These correlations confound the processes of sexual selection and pose special challenges for their study. Ligurotettix, an unusual genus of gomphocerine grasshoppers in which males defend individual host shrubs as mating territories, have proved to be useful species for investigating these issues.

Female Ligurotettix generally settle on certain host shrubs whose foliage represents high–quality food, which may promote egg development. Males are usually found on the same set of host shrubs that harbor females. The settlement of adult males, which occurs prior to the seasonal appearance of adult females, is based on the expected value of a shrub as both a female encounter site and a food resource whose consumption could increase male competitive abilities. Males compete for exclusive residence at valuable shrubs by means of early adult maturation, searching mechanisms for finding the shrubs, and aggression. Loud acoustic signaling by the males attracts females and influences their initial settlement among these shrubs.

Despite high levels of aggression, Ligurotettix males congregate on the most valuable host shrubs. Females may prefer congregated males per se, possibly as a means of reducing the costs of selecting males and locating resources. Some findings suggest that males display mutual attraction and exploit this possible female preference.

ABSTRACT

Mate–finding in the large majority of moths is mediated by a long–distance response of males to minute quantities of pheromone emitted by females. Additionally, in many species, males may produce their own pheromone, which is employed after the sexes are brought together. More rarely, males produce acoustic signals and/or a long–distance pheromone. In the latter case, females assume the searching role. The female pheromone systems of the Heteroneura, a group that makes up 99% of extant Lepidoptera, may have had a single origin with relatively little change occurring subsequently, either in the types of chemicals used or in the glandular structures for pheromone production and release. In addition, female signaling appears to be a plesiomorphic trait for the Lepidoptera that likely was lost independently several times among the primitive groups. Recent research points to the female sternum V gland (located on the fifth abdominal sternum), found throughout primitive Lepidoptera, as the most likely evolutionary predecessor of the heteroneuran sexpheromone system. This gland, which is shared with the sister group Trichoptera, also appears to play a defensive role in some species of the two orders. In contrast to the conservation of female pheromone systems, the incidence of male pheromones in moths is exceedingly polyphyletic and labile, suggesting intense and repeated selection for a transient function. Male acoustic signaling, although less prevalent, also appears to have had multiple origins.

ABSTRACT

Fig–pollinating and fig–parasitizing wasps are integral parts of one of the most fascinating plant–insect interactions known. Moreover, studies of these wasps have been instrumental in developing and refining ideas concerning the influence of population structure and inbreeding on shaping the outcome of kin selection. We present data compiled from six studies spanning five continents that relate brood sex ratios with foundress number in 24 pollinator species. All predictions of local mate competition (LMC) and inbreeding theory are at least qualitatively supported. Additionally, the sex ratios produced by single foundresses of any given species appear to be influenced by brood size and the frequency of multiple foundress broods in that species. We then consider the assumptions underlying the testing of the specific LMC model and consider the relative merits of observational and experimental tests of the theory. Furthermore, we discuss the existing studies of the parasitic wasp species that have addressed the unusual morphological and behavioral polymorphisms for flightlessness and lethal combat that are found in the males of these species. These differences appear to be influenced by the parasites' population structure and density, although other factors are also implicated. Finally, we compare the nature of the support for LMC theory from fig–pollinating wasps with that from the parasitoid wasp Nasonia vitripennis, and suggest future lines of research.

ABSTRACT

Butterflies display a variety of sexual differences in size and morphology beyond those found in the gonads and genitalia. The size and nature of such differences can be explained as (1) the result of selection pressures acting on one or both sexes that are a function of these differences, or (2) as the incidental consequence of selection acting independently on each sex. This chapter reviews various attempts to relate mating–system structure and ecology to these explanations for sexual dimorphism in butterflies. Females are usually larger than males in butterflies; although there are positive size–fecundity relationships in females, the patterns of selection on male size are not understood well enough to explain this pattern. Body and wing shape reflect male mate–locating tactics, but selection pressures shaping female wing and body shape characteristics are poorly known. Sexual selection still appears to be a likely explanation for the elaborate colorations, scent–pro – ducing, and sensory structures in males, although there is clearly more work to be done. These sexual differences all appear to be the products of selection acting independently on the sexes, whereas sexual differences in eclosion patterns might be explained by selection for specific sexual differences in eclosion dates.

INTRODUCTION

A variety of sexual differences in morphology, beyond the gonads and genitalia, are common in butterflies. These include differences in wing color, wing shape, body size, body proportions, sensory structures, foreleg development, and signal–producing structures (Fig. 15–1).

ABSTRACT

Two sympatric species of Zoraptera in central America, Zorotypus barberi Gurney and Z. gurneyi Choe, exhibit distinctively divergent mating behaviors before, during, and after copulations. The mating system of Z. barberi is essentially polygynandry in which both males and females mate with multiple mates. Males of Z. barberi perform elaborate precopulatory courtship involving courtship gifts, provide extra stimulation during copulation, and continue to court for additional copulations. Females appear to exert almost exclusive control over mating by being able to reject males at any point during the entire mating episode. In addition to deciding with whom to mate and how long each copulation lasts, Z. barberi females also control the frequency of copulations. They can mate with one male repeatedly, with different males, or both. Among the hypotheses examined, the material–benefit, postcopulatory female choice, sperm–supply, and fertilization–enhancement hypotheses, or some combinations of them, appear to provide good explanations for the observed mating variations in Z. barberi. Alternatively, repeated mating may be a result of ‘parceling’ of courtship gifts by males to guard females for a longer period of time. In Z. gurneyi, males gain considerable control over mating by establishing dominance hierarchies among themselves and thus predetermining female mating decisions to a certain degree. Zorotypus gurneyi males display no apparent precopulatory courtship; once genital coupling is made, they are able to prolong copulations by everting much of their internal genitalia into the female. After copulations, dominant Z. gurneyi males continue to protect their harems of females from other males.

ABSTRACT

Water striders (Heteroptera: Gerridae) exhibit two different types of mating behavior. The most common mating system (type I) is characterized by strong apparent conflicts of interest between the sexes, and conspicuous pre– and postcopulatory struggles. Some species exhibit a mating system that involves much less apparent conflict (type II) and lack the intense copulatory struggles.

I argue that the predominant mating system in water striders is a direct consequence of sexual conflicts over mating decisions. Matings involve high costs to females (increased predation risk and energetic expenditure) but few, if any, balancing direct benefits. Sperm–displacement rates are high, and males thus gain from rematings. Mating frequencies are high; females mate multiply for reasons of convenience. In these species, males are considered to have ‘won’ the evolutionary conflict over the mating decision in the sense that they have made acceptance of superfluous matings ‘the best of a bad job’ for females, by evolving behavioral and morphological traits that make it costly for females to reject males attempting copulations. Females, however, have apparently evolved a variety of counteradaptations to male harassment, to gain control over mating. Further, I suggest that sexual conflict may have played a crucial role in the evolution of type II matings from type I matings.

ABSTRACT

The term ‘swarm’ has been applied to a variety of aerial mating systems. All are supposedly non–resource–based, although their relationship to resources is sometimes ambiguous. There are several selective contexts for mate choice. The choice of swarm markers has been implicated in species isolation. However, certain swarm markers are used by multiple species, which suggests that qualities other than specificity are important. In some instances, species appear sequentially at a marker, and there is evidence that not all times of day are equally valuable for swarming. It is not clear whether species compete for a universally best time. Swarms themselves, as well as markers, can attract participants, and a swarm's size can contribute to its attractiveness. The position of an insect within a swarm might influence its sexual opportunities. In species where male size is positively correlated with reproductive success, there is an instance where larger individuals occupy certain parts of the swarm. There are more observations of homogeneous size distributions in swarms, although in some species from several families of Diptera, the smallest males swarm very little or not at all. Presumably, they lack the energy resources to compete with larger males. Swarming insects may emit sexual signals. Pheromones seem to be rarely used, perhaps because of difficulties in determining the source of the signal. Visual signals are the easiest to trace to their sender, and furthest projected. Vision seems to be the paramount sense in swarming species.

ABSTRACT

Parasitoid wasps are a large group of hymenopteran insects whose larvae develop by feeding on the bodies of other insects. The spatial distributions of both the hosts and the parasitoid larvae influence the mating systems found in these wasps. Specifically, there is a strong tendency towards mating at the emergence site in species whose offspring develop in gregarious clutches and in species that attack clumped hosts. The genetic and sex–determination systems of parasitoids also influence their mating systems. All sexual parasitic wasps are haplodiploid, with unfertilized eggs becoming males. Thus females can produce male offspring without mating. Some species also show complementary sex determination (CSD) with sex determined by the segregation of alleles at a highly polymorphic sex determination locus. A consequence of this is that inbreeding leads to the production of sterile diploid males. There is therefore selection for females to avoid inbreeding in species with CSD and this is achieved via a premating refractory period in Bracon hebetor. However, we also expect sexual conflict with respect to inbreeding as males are probably selected to take all available mating opportunities.

While laboratory studies of parasitoids have yielded considerable insights, there is a need for more field data on mating systems. Laboratory studies are also needed to help delimit the distribution of CSD, and to investigate patterns of sperm use and mate choice.

ABSTRACT

Females can have important, but often underestimated effects on the likelihood that any given copulation will result in fertilization of their eggs. Examples of at least 15 different processes that occur during or after intromission, and in which females can selectively favor one male's chances of paternity over those of another, are given for insects and arachnids.

Two general phenomena suggest that such ‘cryptic’ female choice is not a rare biological curiosity, but rather a widespread and common phenomenon. Male courtship behavior in insects and spiders often (probably usually) begins or continues after intromission has occurred; the most likely explanation of this otherwise paradoxical behavior is that it serves to influence cryptic female choice. In addition, male seminal products in insects and ticks commonly influence several aspects of female reproductive physiology. Several kinds of evidence indicate that these male products have evolved under sexual selection, usually as triggering mechanisms rather than as nutrients. They may constitute ‘chemical genitalia’ that influence cryptic female choice.

Several widely held ideas about sexual selection and courtship should be modified to take into account the fact that females are less passive in male–female interactions than has previously been supposed.

ABSTRACT

Traditionally, students of odonate reproductive behavior have focussed on how males compete for access to mates and fertilizations. This tendency has yielded considerable information on male reproductive strategies and on the proximate and ultimate mechanisms involved in malemale competition, but has left numerous gaps in our knowledge of other aspects of odonate mating systems.

We review relevant aspects of odonate biology and examine the extent to which current data on mating patterns support predictions arising from sexual selection theory. Although long–term studies offer some such support, they also indicate that natural selection for longevity and stochastic factors such as weather play critical roles in influencing reproductive success. Relatively little of the variance in male reproductive success in odonates has been traced to variance in male phenotype.

We emphasize the role of females as determinants of odonate mating patterns and discuss sexual conflicts of interest over mating, fertilization, and oviposition decisions. Finally, we explore ways in which natural selection underlies female mating decisions and how larval and adult ecology interact to influence adult reproductive behavior.

INTRODUCTION

The study of mating systems is the study of the behavioral, physiological, and ecological factors that underlie predictable patterns of male and female interactions during reproduction. Much of the literature on mating systems emphasizes male–male competition and its effects on male morphology and behavior. However, fertilization success of males cannot be explained solely by pre– and postcopulatory interactions of males or their gametes (see Alexander et al., this volume).