I. the origin of species by means of natural selection

Mate choice by males has been recognized at least since Darwin's time, but its phylogenetic distribution and effect on the evolution of female phenotypes remain poorly known. Moreover, the relative importance of factors thought to underlie the evolution of male mate choice (especially parental investment and mate quality variance) is still unresolved. Here I synthesize the empirical evidence and theory pertaining to the evolution of male mate choice and sex role reversal in insects, and examine the potential for male mating preferences to generate sexual selection on female phenotypes. Although male mate choice has received relatively little empirical study, the available evidence suggests that it is widespread among insects (and other animals). In addition to 'precopulatory' male mate choice, some insects exhibit 'cryptic' male mate choice, varying the amount of resources allocated to mating on the basis of female mate quality. As predicted by theory, the most commonly observed male mating preferences are those that tend to maximize a male's expected fertilization success from each mating. Such preferences tend to favour female phenotypes associated with high fecundity or reduced sperm competition intensity. Among insect species there is wide variation in mechanisms used by males to assess female mate quality, some of which (e.g. probing, antennating or repeatedly mounting the female) may be difficult to distinguish from copulatory courtship. According to theory, selection for male choosiness is an increasing function of mate quality variance and those reproductive costs that reduce, with each mating, the number of subsequent matings that a male can perform ('mating investment') Conversely, choosiness is constrained by the costs of mate search and assessment, in combination with the accuracy of assessment of potential mates and of the distribution of mate qualities. Stronger selection for male choosiness may also be expected in systems where female fitness increases with each copulation than in systems where female fitness peaks at a small number of matings. This theoretical framework is consistent with most of the empirical evidence. Furthermore, a variety of observed male mating preferences have the potential to exert sexual selection on female phenotypes. However, because male insects typically choose females based on phenotypic indicators of fecundity such as body size, and these are usually amenable to direct visual or tactile assessment, male mate choice often tends to reinforce stronger vectors of fecundity or viability selection, and seldom results in the evolution of female display traits. Research on orthopterans has shown that complete sex role reversal (i.e. males choosy, females competitive) can occur when male parental investment limits female fecundity and reduces the potential rate of reproduction of males sufficiently to produce a female-biased operational sex ratio. By contrast, many systems exhibiting partial sex role reversal (i.e. males choosy and competitive) are not associated with elevated levels of male parental investment, reduced male reproductive rates, or reduced male bias in the operational sex ratio. Instead, large female mate quality variance resulting from factors such as strong last-male sperm precedence or large variance in female fecundity may select for both male choosiness and competitiveness in such systems. Thus, partial and complete sex role reversal do not merely represent different points along a continuum of increasing male parental investment, but may evolve via different evolutionary pathways.

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The evolution of male mate choice in insects: a synthesis of ideas and evidence.

Chemical signals are omnipresent in sexual communication in the vast majority of living organisms. The traditional paradigm was that their main purpose in sexual behaviour was to coordinate mate and species recognition and thus pheromones were conserved in structure and function. In recent years, this view has been challenged by theoretical analyses on the evolution of pheromones and empirical reports of mate choice based on chemical signals. The ability to measure precisely the quantity and quality of chemicals emitted by single individuals has also revealed considerable individual variation in chemical composition and release rates, and there is mounting evidence that prospecting mates respond to this variation. Here, we review the evidence for pheromones as indicators of mate quality and examine the extent of their use in individual mate assessment. We begin by briefly defining the levels of mate choice--species recognition, mate recognition and mate assessment. We then explore the degree to which pheromones satisfy the key criteria necessary for their evolution and maintenance as cues in mate assessment; that is, they should exhibit variation across individuals within a sex and species; they should honestly reflect an individual's quality and thus be costly to produce and/or maintain; they should display relatively high levels of heritability. There is now substantial empirical evidence that pheromones can satisfy all these criteria and, while measurements of the actual metabolic cost of pheromone production remain to some degree lacking, trade-offs between pheromone production and various fitness-related characters such as growth rate, immunocompetence and longevity have been reported for a range of species. In the penultimate section, we outline the growing number of studies where the consequences of chemical-based mate assessment have been investigated, specifically focussing on the reported direct and genetic benefits accrued by the receiver. Finally, we highlight potential areas for future research and in particular emphasise the need for interdisciplinary research that combines exploration of chemical, physiological and behavioural processes to further our understanding of the role of chemical cues in mate assessment.

The role of chemical communication in mate choice.

To date, learning has been demonstrated in six orders of insects with phytophagous habits. Most examples of learning in these orders have come to light relatively recently [all but a few since the last review of learning in the Annual Review of Entomology 17 years ago (3)], and many more will surely be uncovered. Still, the study of learning in other insects such as the social Hymenoptera remains far more advanced than in phytophagous insects. In this review, work on learning in phytophagous insects is placed into the broader perspective of learning in a variety of insects including bees and parasitic wasps. Although historically the study of learning in phytophagous insects has emphasized the acquisition of host resources for feeding and oviposition, we believe that, as in bees and wasps, learning impinges on almost every aspect of the natural history of a phytophagous insect. Following discussion of the definition of learning, the natural history of learning, and the host stimuli involved in learning, we review the ecological significance of learning with respect to both the traditional categories erected by behaviorists and the more recent concept of programed learning developed by ethologists. Finally, we evaluate critically hypotheses about the evolution of learning and suggest approaches for future research.

Ecological and evolutionary aspects of learning in phytophagous insects

Learning and memory, defined as the acquisition and retention of neuronal representations of new information, are ubiquitous among insects. Recent research indicates that a variety of insects rely extensively on learning for all major life activities including feeding, predator avoidance, aggression, social interactions, and sexual behavior. There is good evidence that individuals within an insect species exhibit genetically based variation in learning abilities and indirect evidence linking insect learning to fitness. Although insects rely on innate behavior to successfully manage many types of variation and unpredictability, learning may be superior to innate behavior when dealing with features unique to time, place, or individuals. Among insects, social learning, which can promote the rapid spread of novel behaviors, is currently known only from a few well-studied examples in social Hymenoptera. The prevalence and importance of social learning in insects are still unknown. Similarly, we know little abo...

Evolutionary biology of insect learning

The roles of seasonality, host synchrony, and behaviour in the evolutions and distributions of nest parasites in hymenoptera (insecta). with special reference to bees (apoidea)

Males of the solitary sweat bee, Nomia triangulifera, patrol over large areas where thousands of females emerge, searching for receptive females. The daily operational sex ratio is strongly male-biased. Males contact dead, frozen (untreated) females more frequently than they contact females which were washed in hexane, showing that olfactory cues are utilized in mate-finding. A major source of female sex pheromone is in the head. Male pouncing on females is temporally non-random, indicative of group stimulation. Bioassays show that newly emerged females are more attractive to males than are older pollen-collecting females. Female odors are individually distinctive, based on male responses, and there is much variation among females in their attractive properties. Male responses to female odors suggest that learning is important for mating in natural populations. In contrast, the following hypotheses are unlikely to account for the observed behavior: (1) dissipation of female odors; (2) site learning and avoidance behavior by males; (3) decay of male motivation; or (4) male-produced repellents effective against other males. Laboratory and field studies show that female Lasioglossum figueresi produce individually-distinctive odors, which are attractive to males. There is considerable inter-individual variation among females in their attractiveness to males among sexually immature females. Male responses to female odors decay over the course of the presentation, suggesting the importance of learning in natural populations, although several alternatives could not be tested.

Attraction and learning in mate-finding by solitary bees, Lasioglossum ( Dialictus ) figueresi Wcislo and Nomia triangulifera Vachal (Hymenoptera : Halictidae)

The nesting biology of a mainly solitary bee,Lasioglossum (Dialictus) figueresi, is compared with that of a possible relative and mainly eusocial bee,L. (D.) aeneiventre. These bees nest in the ground in highly disturbed areas in the Meseta Central of Costa Rica. Information is provided on social organization, male production, diel and seasonal activity patterns, pollen utilization, natural enemies and nest architecture. 
L. (D.) figueresi nests within aggregations in vertical earthen banks, and 80–90 % of females are solitary during the nest-provisioning phase. Social nests contain two (or rarely three) females which may be either equal or unequal in reproductive status (i.e. mated with developed ovaries or not). Solitary nests and two-female nests do not experience different rates of parasitism. Mid-way through the dry season, females cease provisioning at a time when otherL. (Dialictus) remain active. Females typically remain within their nests, although they occasionally forage for nectar. This behavior is similar of that of “spring gynes” of temperate eusocial species. The egg-to-adult developmental rate ofL. (D.) figueresi is unusually slow for halictine bees, however, so that all the adult females die before their brood eclose in April and May, precluding overlap of generations. The eclosed offspring remain in open cells within their natal nests until mid-June, when both males and females emerge to mate. These newly mated females either establish new nests or re-use old ones. 
L. (D.) aeneiventre nests within aggregations in horizontal ground or in vertical banks. A foundress female digs a nest at the beginning of the dry season, although some re-activate old nests. Foundress nests develop into colonies with various kinds of social organization. In contrast toL. (D.) figueresi, L. (D.) aeneiventre is active nearly all year round, except during periods of heavy rain, and produces up to three broods per year. Sweat bees (Hymenoptera: Halictinae) are a socially heterogeneous group of mainly ground-nesting bees which are abundant world-wide. Intra-specific variation in social behavior is prevalent both within and among populations, presumably indicating social and environmental control of behavioral modifications (see e.g. Sakagami and Munakata, 1972; Eickwort, 1986; Packer, 1990; Yanega, 1988; reviewed in Michener, 1990). The initial stages of hymenopteran social evolution are represented by solitary individuals and those in undifferentiated societies, yet their biology is not well known, as is true for the numerous tropical halictine species or populations (see Michener, 1990). The subgenusDialictus ofLasioglossum is a primarily New World group of several hundred species (Moure and Kurd, 1987). These bees are monotonously similar in structure and appearance, yet diverse in social behavior. FemaleLasioglossum (Dialictus) figueresi are usually solitary, and structurally are very similar to their social relativeL. (D.) aeneiventre (Wcislo, 1990 a). The systematic placement of these species with respect to otherL. (Dialictus) is uncertain, but they have no obvious affinities to other recognized species groups (G. C. Eickwort, pers. comm.). Unusual morphological features, such as large size, yellowish wings and pubescence, and features of the genital organs, may indicate thatL. (D.) figueresi is the more derived of the pair, and may therefore be secondarily solitary, as is known for other sweat bees (Packer, 1991).

Nesting biology of tropical solitary and social sweat bees, Lasioglossum (Dialictus) figueresi Wcislo and L. (D.) aeneiventre (Friese) (Hymenoptera: Halictidae)

Sweat bees [Lasioglossum (Dialictus) figueresi] returning to their nests were not disturbed if small-scale landmarks were added near nests before bees made orientation flights. Landmarks added after orientation flights delayed bees in locating nests when they returned. Spatially displacing landmarks had no effects on bees returning to their nests. Nest entrances usually had conspicuous turrets, but these were not required for nest recognition. Turrets provided some cues concerning nest identity since searching bees preferentially contacted their own turrets over alien ones. Swabbing the inner lining of a nest tunnel with hexane significantly delayed the bee's entry into the nest, but distilled water or an equal amount of hexane applied to the outside of the nest had no effect. The delay induced by a hexane wash was reduced significantly by placing the bee's unwashed turret on the nest entrance. Adding whole-body hexane extracts from probably unrelated females to nest entrances significantly delayed bees' entering nests.



A review of mechanisms for nest recognition within Apoidea shows that to date olfactory mechanisms are more prevalent among bees (Apiformes) than wasps (Spheciformes). This pattern may be an artifact of the little information available on wasps. If substantiated, then known cases of olfactory nest recognition generally co-occur with a tendency toward social evolution within Apoidea, supporting a hypothesis proposed by Holldobler & Michener (1980).

Nest localization and recognition in a solitary bee, Lasioglossum (Dialictus) figueresi Wcislo (Hymenoptera : Halictidae), in relation to sociality

Results from experiments on the role of learning in the mating biology of a sweat bee, Lasioglossum zephyrum (Hymenoptera: Halictidae), are described in this paper. Male learning of individual female odors is important in natural populations (Table 1), as has been shown in the laboratory. Four other hypotheses are unlikely to account for the observed behavior: (1) Female odors dissipate rapidly; (2) Males learn and then avoid the study area; (3) Males or females produce repellents which are effective against other males; or (4) males recognize their own odor on previously-contacted females, which they subsequently avoid. Regarding questions of “male preference” and “optimal outbreeding,” Tables 2 and 3 show there are no consistent preferences for more novel or less novel female odors.

William T. Wcislo

Papers

The roles of seasonality, host synchrony, and behaviour in the evolutions and distributions of nest parasites in hymenoptera (insecta). with special reference to bees (apoidea)

Attraction and learning in mate-finding by solitary bees, Lasioglossum ( Dialictus ) figueresi Wcislo and Nomia triangulifera Vachal (Hymenoptera : Halictidae)

Nesting biology of tropical solitary and social sweat bees, Lasioglossum (Dialictus) figueresi Wcislo and L. (D.) aeneiventre (Friese) (Hymenoptera: Halictidae)

Nest localization and recognition in a solitary bee, Lasioglossum (Dialictus) figueresi Wcislo (Hymenoptera : Halictidae), in relation to sociality

The role of learning in the mating biology of a sweat bee Lasioglossum zephyrum (Hymenoptera: Halictidae)