Sexual Selection (Insects)

Sexual selection depends on the success of certain individuals over others of the same sex, in relation to the propagation of the species; while natural selection depends on the success of both sexes, at all ages, in relation to the general conditions of life. Sexual selection is a struggle between individuals of one sex, generally the males, for the possession of the other sex. The result is not death to the unsuccessful competitor, but few or no offspring…. Charles Darwin (1859)

HISTORICAL PERSPECTIVES

Darwin proposed the concept of sexual selection to explain the sexually dimorphic characters he observed in a wide diversity of organisms. He introduced the concept in On the Origin of Species in 1859 and further expanded on his theory in The Descent of Man and Selection in Relation to Sex in 1871. The development of the theory has been rich in controversies and so continues to the present, primarily because of the uncertainty over how much of the sexual dimorphism present in animals is the result of natural selection as opposed to sexual selection.
Notable theoreticians and evolutionary biologists severely criticized Darwin’s theory of sexual selection and argued that sexual selection was less important than natural selection in bringing about evolutionary changes. Until recently, most evolutionary biologists accepted the notion that natural selection is the most dominant force in the evolutionary history of the species. The ubiquity of this view is well understood when one considers the notion that populations could ill afford the incapacity to adjust to the effects of their external environment. Even Darwin stated that “sexual selection will also be dominated by natural selection tending towards the general welfare of the species.” Nevertheless, Darwin stood firm in his ideas and stated that his “conviction of the power of sexual selection remains unshaken. ”


THEORETICAL CONSIDERATIONS

Anisogamy and Parental Investment

The evolutionary origins of differences between the male and female sexes lie in what is referred to as anisogamy, which is the difference in gamete size between the two sexes. Females generally produce a few but large gametes, whereas males produce large numbers of much smaller gametes. Furthermore, such sex bias in gamete size is also characteristic of the initial stages of the evolutionary differences in parental investment, because the production of large gametes requires greater energetic investment by the female than the smaller male gametes. In most species, the male’s investment ends with fertilization, while that of females may continue throughout the developmental period of the zygote, embryo, and other immature stages of the organism. Consequently, the limited number of gametes and the greater parental investment of the females result in an asymmetry in the degree of sexual selection between the two sexes. One might expect females to be generally less sexually selected but more selective in their choice of males (but see later), with males being under stronger sexual selection, hence attempting to mate with as many females as possible. It is thought that the males with the best territories, the most elaborate structures, the most attractive displays (i.e., secondary sexual traits), and so on will mate more frequently and therefore will leave more offspring. In terms of “investment” then, since it costs females much more to produce fewer large gametes than it does males, which produce lots of small gametes, females must “choose” mates that will produce the highest quality offspring (genetically).

Competition for Mates

It has been suggested that Darwin’s concept of sexual selection may be subdivided into two aspects: “intrasexual selection,” which involves competition between members of the same sex for individuals of the opposite sex, and “epigamic selection,” which is the preferential choice of mates by one sex relative to the other. Intrasexual selection is most evident in males and perhaps can be best illustrated in species that display lek mating behavior. In such species, males compete among themselves for territories to which receptive females are attracted strictly for the purpose of mating (i.e., the territories do not provide other resources such as food or egg-laying substrates). In some species, a dominance hierarchy is established among the males that may be participants in a lek system and as a rule, the males able to occupy and defend the “best” territories will have access to most of the females that arrive at the lek. Epigamic selection, which is also referred to as “intersexual selection,” is primarily an attribute of females, since the female sex ultimately discriminates among males and exercises choice of mating partners. Curiously, in most lek species, even though the most dominant males are successful in defending what seem to be the best territories in the lek system (as evidenced by the number of females that arrive at the territories of such males), males nevertheless perform an elaborate courtship ritual before mating occurs. Sometimes a female indeed rejects a dominant male’s courtship and mating attempts, moves to an adjacent territory, and eventually mates with a subordinate male. Such occurrences illustrate that although fierce intrasexual selection among males can occur in competition for mating territories, epigamic selection based on female choice is the ultimate determinant of mating success among males, and thus intra-sexual selection is not necessarily linked or correlated with epigamic selection. That is, a dominant male that is able to occupy and defend a prime mating territory, must, nevertheless perform courtship displays, which may or may not be acceptable to receptive females.

Runaway Sexual Selection Model

Darwin himself recognized a serious gap in his ideas of sexual selection and stated: “Our difficulty in regard to sexual selection lies in understanding how it is that the males which conquer other males, or those which prove the most attractive to the females, leave a greater number of offspring to inherit their superiority than their beaten and less attractive rivals. Unless this result does follow, the characters which give to certain males an advantage over others could not be perfected and augmented through sexual selection.” Critics ridiculed Darwin’s ideas and sarcastically implied that Darwin would not be able to prove his theory.
The oftentimes sarcastic attacks against Darwin’s sexual selection theory challenged theoreticians to develop alternative hypotheses for the evolution of female preference for, and the evolution of, secondary sexual traits in males. The most notable of these hypotheses is the ” runaway selection” model, according to which it was inferred that the evolution of a sexually dimorphic character in males could result in a correlated response in the female’s preference for that character. The model predicted that female choice and male characteristics influenced by sexual selection would coevolve very rapidly in an interbreeding population. The runaway selection model presumed that two forces act to counterbalance the runaway process of sexual selection. That is, female preference for a certain male character, whether morphological or behavioral, tends to select for extreme forms of that character until natural selection exerts its forces to maintain the optimum male phenotype that is best able to survive in its particular environment. In an article published in 1972, Ernst Mayr stated that “natural selection will surely come into play as soon as sexual selection leads to the production of excesses that significantly lower the fitness of the species.”
The paradox of the runaway sexual selection model is that the opposing forces of sexual selection for elaboration of conspicuous male traits and natural selection, which maintains the optimum condition for the particular environment, result in reduced genetic variation for such male characters (Fig. 1). However, without genetic variation, selection can no longer occur; and unless secondary sexual characters either are linked to or are pleiotropic effects of other components of fitness, such conspicuous characters would be energetically costly to produce, and individuals possessing such traits would be in greater danger of predation.

The Differential Selection Model

In 1989, in an attempt to provide an alternative explanation for the maintenance of secondary sexual characters observed in males, Kaneshiro proposed a model based on his research on the mating behavior of Hawaiian Drosophila species. He suggested that there is a range of male mating types segregating within an interbreeding population. That is, some males in the population are highly successful in mating and often accomplish the majority of the matings in the population. Other males are less successful and in fact may not mate at all, despite being given the opportunity to do so with several receptive females. Similarly, among females, there are those that exhibit higher levels of mating receptivity thresholds and strongly discriminate against most of the males in the population. In the
The runaway sexual selection model: (A) distribution of mating types segregating in the population, (B) strong sexual selection and elaboration of male trait that confer mating success, and (C) opposing forces of natural selection, which select for optimum phenotype for a particular environment.
FIGURE 1 The runaway sexual selection model: (A) distribution of mating types segregating in the population, (B) strong sexual selection and elaboration of male trait that confer mating success, and (C) opposing forces of natural selection, which select for optimum phenotype for a particular environment.
same population, there are also females that exhibit lower receptivity thresholds and seem to accept the courtship overtures of most of the males in the population.
Observations of mating experiments of Hawaiian Drosophila both in the laboratory and in the field indicate that the most likely matings are between males that are most successful in satisfying the courtship requirements of females and females that are not extremely choosy in selecting mating partners. The genetic correlation between these two behavioral phenotypes in the two sexes (i.e., highly successful males and less choosy females) generates the entire range of mating types in both sexes in subsequent generations (Fig. 2). In this model then, there is differential selection for opposite ends of the mating distributions in the two sexes and therefore, sexual selection itself serves as the stabilizing force in maintaining a balanced polymorphism in the mating system of the population. Hence, it is not necessary to invoke the forces of natural selection to counterbalance the elaboration of secondary sexual characters as required in the runaway sexual selection model.
Differential sexual selection model, which shows that matings between less choosy females and successful males generate the entire range of mating types in each successive generation.
FIGURE 2 Differential sexual selection model, which shows that matings between less choosy females and successful males generate the entire range of mating types in each successive generation.

SEXUAL SELECTION IN INSECTS

Different patterns of sexual selection that have been observed can be illustrated by descriptions of sexual selection in a few insect species. This is certainly not a comprehensive review, since space constraints allow only a very few examples to be discussed. Several topics present a more in-depth discussion of sexual selection systems in insects, and the reader is referred to such treatments.

Lek Behavior in Hawaiian Drosophila and Other Dipteran Species

In an article published in 1997, Shelly and Whittier list the following criteria in defining a lek species: “(1) the absence of male parental care, with males contributing nothing but gametes to the female;
(2) the existence of a mating arena in which most matings occur;
(3) male territories that contain no resources vital to females; and
(4) the opportunity for females to freely select a mate in the arena.” These authors also recognize two types of male mating aggregations involved in lek mating species: substrate-based, where males spend most of the time perched at stations or territories to which females are attracted for mating (although mating may occur in the air), and aerial aggregations or swarms, in which males are usually in continuous flight and matings are typically initiated in the air.
In the mating system of the Hawaiian Drosophilidae, males take up station either on the underside of leaves, one male to a leaf, or on branches of understory shrubs. Resident males aggressively defend territories from intruding males with fierce battles (Fig. 3), which in some species resemble sumo wrestling bouts. In the lek mating system of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae), males occupy and aggressively defend the underside of leaves of host plants as mating territories to which females are attracted solely for the purpose of mating. Once a female has arrived at the mating arena, the males of both the Mediterranean fruit fly and the drosophilids display complex courtship behaviors, which may or may not result in acceptance by the female. This means that successful aggressive behavior is not necessarily linked to or correlated with successful mating behavior. That is, a male that is successful in occupying and defending prime mating territories still must perform a courtship sequence that is acceptable by the females to ensure mating success. In some cases, the alpha male (i.e., the male that is most successful in defending a prime mating territory) is not successful in mating despite numerous visits by receptive females.
Males of the native Hawaiian Drosophila, D. heterone-ura, in head-to-head, wingtip-to-wingtip posture, defending a territory to which females are attracted solely for the purpose of mating. The "hammerhead" shape of the males appears to be a result of sexual selection for this behavioral display among males in a lek mating system.
FIGURE 3 Males of the native Hawaiian Drosophila, D. heterone-ura, in head-to-head, wingtip-to-wingtip posture, defending a territory to which females are attracted solely for the purpose of mating. The “hammerhead” shape of the males appears to be a result of sexual selection for this behavioral display among males in a lek mating system.
Courtship display of a native Hawaiian Drosophila, D. clavisetae. While in a "scorpion-like" posture, the male produces a pheromone bubble and wafts (a row of apically flattened bristles near the terminal end of the abdomen serves as a "fan") the chemical stimulant toward the female by vibrating his abdomen in an up-and-down motion toward the female. The courtship " dance " also involves visual cues (striking white face and wing markings are sexually dimorphic characters), tactile cues (female " kisses " the extended proboscis of the male), as well as acoustical cues. Despite the complex courtship displays and considerable effort on the part of the male, sexual selection via female choice (i.e., epigamic selection) plays a powerful role in determining mating success.
FIGURE 4 Courtship display of a native Hawaiian Drosophila, D. clavisetae. While in a “scorpion-like” posture, the male produces a pheromone bubble and wafts (a row of apically flattened bristles near the terminal end of the abdomen serves as a “fan”) the chemical stimulant toward the female by vibrating his abdomen in an up-and-down motion toward the female. The courtship ” dance ” also involves visual cues (striking white face and wing markings are sexually dimorphic characters), tactile cues (female ” kisses ” the extended proboscis of the male), as well as acoustical cues. Despite the complex courtship displays and considerable effort on the part of the male, sexual selection via female choice (i.e., epigamic selection) plays a powerful role in determining mating success.
Thus, at least for the drosophilids and tephritid fruit flies, although success in intrasexual selection among males may mean increased opportunity to encounter receptive females, the ultimate criterion for successful mating is epigamic selection based on female choice (Fig. 4).

Resource-Based Sexual Selection in the Scorpion fly

The mating system of the scorpion fly, Hylobittacus apicalis (Mecoptera: Bittacidae), provides another excellent example of intra-sexual and epigamic sexual selection. Here intrasexual selection is evidenced by the competition among males for arthropod prey, which are offered to females as nuptial gifts. Males that are able to acquire such resources will have greater access to receptive females. It has also been shown that the size of the nuptial prey plays an important role in epigamic selection. Females apparently have the ability to evaluate the males based on the size of the nuptial gift, on which they feed during copulation. Females prefer males with a large prey versus males that offer smaller prey. Such preference results in an increased number of eggs oviposited as well as the survivorship of the female. Essentially, size of prey is correlated with the length of the copulation. It was shown that at least 5 min of mating is required before any sperm is transferred to the female and that copulation duration ranging between 5 and 20 min is directly correlated with the number of sperm transferred. Thus, when a male offers and the female accepts a large nuptial gift, the male is provided an opportunity to transfer a complete quantity of sperm. In some cases, if the prey is large enough, the males may end the mating with the first female to be able to use the prey as a gift for a second female. Furthermore, a male that mates for 20 min or longer introduces a substance into the female’s reproductive tract that renders the female sexually nonreceptive and stimulates oviposition. Females that mate for less than 20 min because of small prey size will continue to seek males with larger prey.
Thus, H. apicalis females may either reject males with small prey or mate with them for only a brief period, feeding on the prey but receiving few or no sperm. Females may then seek males that can offer larger prey, which will increase the likelihood of a sperm transfer adequate to fertilize her full complement of eggs. Such female preference for males that can offer larger, nutrient-rich prey, which influences the number of offspring produced, has clearly shaped the evolution of male behavioral components in this species. Since insect prey is a limited resource, as evidenced by the small number of males (~2-0%) that are carrying prey at any one moment, there is competition among males in securing prey. Males that are successful in securing a gift are not guaranteed to reproduce, since females discriminate against prey-bearing males that offer small prey. On the other hand, males that are able to secure sufficiently large prey may be able to mate with more than one female.
Female choice for prey-bearing males has apparently resulted in the evolution of other male behaviors. For example, it has been shown that males foraging for prey are more prone to predation and that males are 2.3 times more likely to be trapped in spider webs than females. Because hunting for prey can be hazardous, H. apicalis males can employ an alternative tactic of securing prey, namely, thievery. Some males fly to calling males and mimic female behavior— for example, perching next to a prey-bearing male and waiting for the gift to be presented, as if to a real female. If the ruse works, the thief will snatch the prey and use it to attract and feed a female without having to spend energy in a risky search of prey of his own. Thus, it would seem that sexual selection has played an important role not only in the evolution of nuptial gift giving in males but also in the development of female-mimicking behavior and prey stealing as an alternative strategy to minimize predation pressure.

THE ROLE OF SEXUAL SELECTION

IN SPECIATION

Two decades ago, Mayr remarked: “Speciation.. .now appears as the key problem of evolution. It is remarkable how many problems of evolution cannot be fully understood until speciation is understood.. ” Over the past 20 years, there has been renewed interest in the process of speciation, initially to address arguments advanced by the proponents of the punctuated equilibrium model of macroevolution but also to revisit the definition of a species. At least two topics address questions of speciation and the evolutionary processes of species as populational units of biological diversity. It is not the intent of this topic to discuss the various models of speciation. Speciation and Its Consequences edited by Otte and Endler, published in 1989, and Speciation and the Recognition Concept edited by Lambert and Spencer, published in 1995, offer comprehensive reviews of this topic.
In 1997 Hampton Carson suggested that when demographic circumstances force populations to pass through a size bottleneck, the sexual selection system is temporarily disorganized by genetic recombination and the consequences of small population effects. As the population builds back up to restore efficient mate choice, novel genetic recombinants may be generated that in turn may lead to “novel selective change over a relatively small number of generations.” and that “the new population may thus be driven to undergo progressive genetic change under sexual selection.”
Based on results of mating experiments on Hawaiian Drosophila species, Kaneshiro formulated a hypothesis, that may provide an intuitive explanation for what Carson referred to as the “driver of genetic change.” Kaneshiro suggested that under conditions of drastic population reduction, there is even stronger selection for less choosy females in the population, since highly discriminant females may never encounter males that are able to satisfy their courtship requirements. If the bottleneck condition persists over a few generations, there will be a shift in the distribution of mating types in the population until a significant increase in frequency of less choosy females in the population has occurred (Fig. 5). Such a shift in the distribution of mating types may be accompanied by a corresponding shift in the gene frequencies in the population, resulting in the destabilization of the coad-apted genetic systems that had evolved in the population. The resulting destabilized genetic environment thus sets the stage for genetic changes conducive to the speciation process. That is, the breakup of coadapted sets of genes allows the generation of novel genetic recom-binants, some of which may be better adapted to the environmental conditions that led to population reduction. Thus, the dynamics of the sexual selection system can play an extremely important role in the speciation process as well as in the maintenance of genetic variability in the population on which the forces of natural selection can operate.
In the evolution of island biota such as that of the Hawaiian Islands, the most likely mode of speciation is what evolutionary biologists call founder event speciation. For insect groups such as the Hawaiian Drosophilidae, the most probable scenario is that a single
Under conditions of reduced population, there is strong selection for less choosy females, since choosy females may never encounter males able to satisfy their courtship requirements.
FIGURE 5 Under conditions of reduced population, there is strong selection for less choosy females, since choosy females may never encounter males able to satisfy their courtship requirements.
fertilized female may be blown to an adjacent island, there to establish a new colony. For a number of generations, during the initial stages of colonization when the population size is small, there would be strong selection for females that are less choosy in selecting mates, once again, because females that are too choosy may never encounter males able to satisfy their courtship requirements. Therefore, within a few generations, there would be a shift in the distribution of mating types toward an increased frequency of less choosy females, resulting in a significant shift in gene frequencies followed by a destabilization of the coadapted genetic system. Genetic recombinants better adapted to the new habitat may be generated and strongly selected, especially if these genotypes are linked or correlated with the genotypes of the less choosy females. Thus, at least during the initial stages of colonization immediately following the founder event, the dynamics of sexual selection may play a significant role in generating a genetic environment in the population that is conducive to the formation of new species.

THE ROLE OF SEXUAL SELECTION AND NATURAL HYBRIDIZATION

It has been suggested that the dynamics of the sexual selection process also provides the opportunity for occasional natural hybridization and permits the “leakage” of small amounts of genetic material from a related species without destroying the integrity of the separate gene pools. When the population is small and there is a shift in the distribution of mating types toward an increase in frequency of less choosy females, such females in the population may occasionally accept males of a related species, which may be less susceptible to the environmental stress conditions. Genes that may be resistant to the conditions responsible for reducing the population size may be strongly selected, especially if such genes are linked to the genotypes of the less choosy females. Therefore, natural hybridization as permitted by the sexual selection process may do more than play an important role in replenishing genetic variability that may be lost owing to drift when population size is small; it may also provide a process by which resistant genes are transmitted between populations.

CONCLUDING REMARKS

The differential sexual selection model discussed here and its role in the processes of speciation may provide a possible explanation of how genetic variability may be not only maintained but actually enhanced. The generation of novel genetic recombinants and the selection for genotypes that are better adapted to changing environmental conditions are enhanced by the sexual selection system in the population, especially when subjected to population bottlenecks. It is suggested that sexual selection is a dynamic process, influenced by density-dependent factors, that enables populations to overcome environmental conditions that result in drastic reduction in population size. Shifts in the distribution of mating types when population sizes are small can generate a genetic environment producing novel recombinants able to respond to the environmental stress imposed on the population. Sexual selection influences the levels of genetic variability generated via novel genetic recombinants resulting from a reorganization of the genome, and via natural hybridization that is permitted by the sexual selection model. Thus, the biology of small populations and the dynamics of the sexual selection process are important aspects of evolutionary biology and the biology of insect populations in general. A better understanding of the role of sexual selection would provide important insights into the mechanisms of species formation as well as enabling us to develop more effective management programs, not only for pest populations but also for the conservation of rare and endangered insects.

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