Polymorphism of competition type and its genetics in Callosobruchus maculatus (Coleoptera: Bruchidae)

Callosobruchus maculatus has both contest and scramble competition strategies. The currently existing theoretical models using game theory suggest that the contest strategy should be selected for. However, most geographic strains of C. maculatus show scramble competition. We experimentally crossed the representative strains of contest and scramble. We expressed the degree of contest competition by a continuous value named the C-value, which ranges from zero (pure scramble) to unity (pure contest). The competition types expressed in the C-value were genetically additive. Their larval developmental rates were negatively correlated with C-values. Multiple-generation experiments of the mixed strains confirmed that there were no overwhelming advantages of contest over scramble type. Most of the mixed strains remained in the intermediate states. We discuss the results in terms of the resource size necessary for developmental success and developmental speed. Received: April 19, 2001 / Accepted: November 2, 2001     

Contest and scramble competitions inCallosobruchus maculatus (Coleoptera: Bruchidae)

Larval competition curves and resource sharing patterns of 5 strains of Callosobruchus maculatus (iQ, yQ, aaQ, wQ, and tQ) were examined. Offspring emergences as a function of the initial larval density were recorded to construct competition curves. Elytron length of emerged adults was used as the indicator of resource sharing patterns among competing larvae inside a bean. In the large beans, strain iQ showed a saturated competition curve and tQ strain showed a humped curve. Competition curves of the other 3 strains (yQ, aaQ, and wQ) were between those two extremes. In the small beans, strains iQ and tQ also showed a saturated and a humped competition curves, respectively, whereas the competition curves of the 3 intermediate scramble strains could not be distinguished from that of the iQ strain. Thus, the classification based on competition curves was sensitive to the resource condition (bean size). In both the large and the small beans, the elytron lengths of iQ strain remained constant irrespective of initial larval density. On the contrary, the elytron lengths of the 4 other strains decreased monotonically with higher initial larval density. Thus, the judgment based on the resource sharing pattern was shown to be robust. Only iQ strain should be designated as a contest type, and the remaining strains as scaramble types. Contest and scramble types in C. maculatus were also compared with those observed in C. analis and C. phaseoli using competition curves, resource sharing patterns, and other physiological characters.     

Wall-making behavior as a proximate mechanism to generate variation in larval competition in Callosobruchus maculatus (Coleoptera: Bruchidae)

Variation from contest to scramble in larval competition types was observed among laboratory lines derived from a geographic strain of Callosobruchus maculatus. In contest competition, only one adult can emerge from a small bean because the successful larva monopolizes resources. In scramble competition, however, multiple adults can emerge from the bean because larvae share resources. To explain the variation in competition types, we used six lines of the geographic strain to test the hypothesis that the larval competition type is determined by the larval behavior of building walls, which prevent larvae from interfering with each other, allowing multiple adults to emerge from a single bean. We also investigated the proportions of wall-making in contest-scramble hybrid lines to test whether the formation of a wall structure was genetically determined. Results support our hypothesis that wall-making behavior determines the type of larval competition within a geographic strain, and that the behavior is genetically determined. Scramble-type lines exhibited higher frequencies of wall-making than contest-type lines when two larvae of the same line infested a bean. Larval competition type and the tendency towards wall formation in contest-scramble hybrid lines ranged intermediate of parental lines. We concluded that the variation in larval competition type is determined by the variation in larval wall-making behavior among laboratory lines derived from the geographic strain. We will discuss the evolution of scramble-type larvae in C. maculatus based on our results.     

Contest and scramble competitions inCallosobruchus maculatus (Coleoptera: Bruchidae) II. Larval competition and interference mechanisms

Competition between contest and scramble strategists was examined using two strains of Callosobruchus maculatus, the contest strain (iQ) and the scramble strain (tQ). The direct larval interference experiment within each strain showed that the contest strain performed strong direct interference throughout its larval stage against the conspecific opponent(s). The scramble strain also performed its interference, but only during the 3rd and the 4th larval stages. The inter-strain larval competition experiments inside a large and small mung bean (Vigna radiata) showed that the contest strain was, in general, superior to the scramble strain in competition, but the competition results were density- and frequency-dependent. In the large beans, the proportion of adult emergence of the contest strain increased with the increase of its own initial density but decreased as the initial density of the scramble strain increased. The shape of the proportion of adult emergence became nonlinear in the small beans. The cause of the complexity of inter-strain competition results was discussed in the light of the difference in larval interference ability between the two strains.     

Avoidance of reproductive interference causes resource partitioning in bean beetle females

Reproductive interference is any interspecific sexual interaction that adversely affects female fitness through indiscriminate reproductive activities. It can be a driving force of resource partitioning in conjunction with resource competition. We previously showed that the bean beetle Callosobruchus maculatus is superior in larval resource competition, but vulnerable in reproductive interference, compared with its congener C. chinensis. We hypothesized that these two species might use two resources differently if one of the resources modified the intensity of reproductive interference or resource competition. We observed that C. maculatus females often enter gaps between beans to avoid mating attempts of heterospecific males, and hypothesized that removing bean gaps would strengthen reproductive interference. Therefore, we provided normal beans with gaps and split beans without gaps to females of the two species housed with conspecific or heterospecific males or no males and compared the number of eggs on each bean type among treatments. Callosobruchus maculatus females housed with heterospecific males were more likely to oviposit on normal beans than C. chinensis females. As a result, more C. chinensis adults hatched from split beans and more C. maculatus hatched from normal beans when females and males of both species were housed together. Thus, oviposition resource partitioning resulted from the combination of female avoidance of reproductive interference and resource competition.     

Competition strategies and correlated selection on responses to polyandry in the seed beetle Callosobruchus maculatus

Abstract Polyandry reflected in multiple mating with different mates is regarded as favoured by natural selection in males but not necessarily in females, where conflicting effects on fitness components can occur. The present study aims to provide empirical evidence to predict which fitness components may be affected in this sexual conflict using a species that demonstrates potential between‐population variation in their resolution: the cowpea weevil Callosobruchus maculatus. Two strains showing contrasting competition outcomes (scramble × contest) and contrasting life‐history strategies based on trade‐offs between longevity and fecundity are crossed for subsequent selection based on larval‐competition strategy, expecting the production of a correlated response to multiple (polyandrous) mating. Such a response is expected because the scramble strain shows high fecundity (and lower longevity) and would benefit from multiple mating, in contrast with the contest strain, which shows high juvenile mortality. The scramble‐selected lines would evolve a response of increased fecundity and reduced longevity under multiple and potentially polyandrous mating but the contest‐selected lines would not respond to multiple (polyandrous) mating. Instead, both scramble‐ and contest‐selected lines show increased fecundity and reduced longevity with multiple (polyandrous) matings, which did not affect egg weight. Indirect benefits of multiple (polyandrous) mating appear to be relevant for lines showing contest competition among juveniles.     

Larval competition within seeds: From the behaviour process to the ecological outcome in the seed beetle Callosobruchus maculatus

Abstract Environmental conditions experienced by organisms during development can have profound impacts on adult fitness and behaviour. Internally feeding larvae unable to leave the seed selected by their mother face limitations of resource suitability and competition. The host seed may guide the larval behaviour within the seed leading to differential intensity of competition and determining its process and outcome, which varies in strains of the legume seed beetle Callosobruchus maculatus (Coleoptera: Bruchidae). However, the intensity, process and outcome of larval competition in different hosts have yet to be simultaneously considered, the objective of the present study. Here we assessed the intensity, process and outcome of intrastrain larval competition as related to host type, and how they are interrelated. Larval competition was faced with two distinct strategies – scramble and contest competition depending on the insect strain and host seed species. The intensity of competition did not show any straight link with the process and outcome of competition. Only a single strain showed a contest competition process with likely interference between larvae, while the four other strains studied showed the process of scramble competition. The process of scramble competition, however, led to variable outcomes in mung beans based on larval competition curves. Such differences were not apparent on cowpea seeds and either the plateau or the peak expected on the larval fitness curves were not reached preventing the distinction of the competition outcome, a likely consequence of the egg laying behaviour of these strains limiting the maximum number of eggs laid per seed. Seed host species rather than seed size are the likely cause of the differences observed from the initial expectation. The strain showing the process of contest competition increased larval fitness with density of larvae emerged per seed regardless of the host species, an unexpected outcome based on theoretical models. In this case the egg laying behaviour of the adult female is probably the main fitness determinant of its progeny.     

Strategic ejaculation and level of polyandry in <Emphasis Type="Italic">Callosobruchus chinensis</Emphasis> (Coleoptera: Bruchidae)

Variation in the level of polyandry of females produces a difference in the risk of sperm competition among males. As a consequence, investment in ejaculate expenditure by males should vary. We compared the number of sperm ejaculated by males into the female reproductive organ of six strains of the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae), when males were reared at different larval densities in a bean. A significant positive correlation was found between the remating frequency of females and the ratio of the ejaculate sizes of high-density and low-density males as a measure of the response to the risk of sperm competition among males. The measure was estimated by dividing the number of sperm ejaculated by males reared at high larval density in a bean with the number of sperm ejaculated by males reared alone. The number of sperm transferred by a male to a female was not correlated with the duration of copulation. The results suggest an evolutionary relationship between ejaculatory expenditure and the level of polyandry in C. chinensis.     

SPERM COMPETITION GAMES: A GENERAL MODEL FOR PRECOPULATORY MALE–MALE COMPETITION

Reproductive males face a trade‐off between expenditure on precopulatory male–male competition—increasing the number of females that they secure as mates—and sperm competition—increasing their fertilization success with those females. Previous sperm allocation models have focused on scramble competition in which males compete by searching for mates and the number of matings rises linearly with precopulatory expenditure. However, recent studies have emphasized contest competition involving precopulatory expenditure on armaments, where winning contests may be highly dependent on marginal increases in relative armament level. Here, we develop a general model of sperm allocation that allows us to examine the effect of all forms of precopulatory competition on sperm allocation patterns. The model predicts that sperm allocation decreases if either the “mate‐competition loading,”a, or the number of males competing for each mating, M, increases. Other predictions remain unchanged from previous models: (i) expenditure per ejaculate should increase and then decrease, and (ii) total postcopulatory expenditure should increase, as the level of sperm competition increases. A negative correlation between a and M is biologically plausible, and may buffer deviations from the previous models. There is some support for our predictions from comparative analyses across dung beetle species and frog populations.     

Contest‐type competition between age classes in scramble‐type Callosobruchus maculatus (Coleoptera: Bruchidae)

We examined the effect of age differences on competition type in individuals of a scramble‐type strain of Callosobruchus maculatus (F.). When oviposition of two individuals on a bean was manipulated to introduce time intervals using two lines with different adult body colors, the frequency of two‐adult emergence decreased with the introduction of sequential oviposition. This result indicates that an age difference between two individuals induces contest competition. The frequency of adult emergence in older individuals decreased, whereas in younger individuals it increased with the introduction of sequential oviposition. Using a dissecting microscope, we observed that bodies of older individuals that died in the bean during the 4‐day oviposition interval were crushed at the pupal stage under the pupal chambers of younger individuals. These results show that an age difference between two larvae in a bean causes contest competition due to one‐sided interference by a younger individual during pupation of an older individual. Based on these experimental results, we discuss the ecological cause of contest competition and the population‐level consequences of identified interactions in scramble‐type C. maculatus.     

Impaired sperm quality,delayed mating but no costs for offspring fitness in crickets winning a fight

The outcome of male–male contest competition is known to affect male mating success and is believed to confer fitness benefits to females through preference for dominant males. However, by mating with contest winners, females can incur significant costs spanning from decreased fecundity to negative effects on offspring. Hence, identifying costs and benefits of male dominance on female fitness is crucial to unravel the potential for a conflict of interests between the sexes. Here, we investigated males' pre‐ and post‐copulatory reproductive investment and its effect on female fitness after a single contest a using the field cricket Gryllus bimaculatus. We allowed males to fight and immediately measured their mating behaviour, sperm quality and offspring viability. We found that males experiencing a fight, independently of the outcome, delayed matings, but their courtship effort was not affected. However, winners produced sperm of lower quality (viability) compared to losers and to males that did not experience fighting. Results suggest a trade‐off in resource allocation between pre‐ and post‐mating episodes of sexual selection. Despite lower ejaculate quality, we found no fitness costs (fecundity and viability of offspring) for females mated to winners. Overall, our findings highlight the importance of considering fighting ability when assessing male reproductive success, as winners may be impaired in their competitiveness at a post‐mating level.     

Male sperm expenditure under sperm competition risk and intensity in quacking frogs

In the frog Crinia georgiana, reproductive behavior comprisesa "guarding tactic," in which males defend spawn sites and attractfemales by calling, and a "sneak tactic," in which males joinspawning pairs. The aims of the present study were to (1) relateejaculate expenditure by "guarding" and "sneak" males to theirprobability of mating with other males present (sperm-competitionrisk), and (2) determine if males adjust their ejaculate expenditureaccording to the number of males involved in a spawning (sperm-competitionintensity). Theory predicts that because sneak males alwaysmate with other males present, they will experience a highersperm-competition risk and should release larger ejaculatesrelative to that of guarding males. However, as the proportionof sneaks in a population increases so does the risk of spermcompetition to guarders, so expenditure by each tactic shouldmove toward equality. Given that the incidence of sneak behavioris high in C. georgiana, guarders and sneaks were expected toexperience similar risks of sperm competition and show similarinvestment in spermatogenesis. Comparison of testes size andejaculate size showed no difference between tactics. Modelsof sperm-competition intensity predict that males should increasetheir ejaculate size when spawning in the presence of one othermale but decrease their ejaculate size when spawning in thepresence of multiple males. Here, males maintained a constantsperm number irrespective of whether a mating involved one,two, or three males. This result suggests that male C. georgianado not facultatively adjust ejaculate investment in responseto fluctuating intensities of sperm competition.     

Contest and scramble competitions in two bruchid species,Callosobruchus analis andC. phaseoli (Coleoptera: Bruchidae)

Larval competition between contest and scramble strategists was investigated using the two bruchid species, C. analis (contest species) and C. phaseoli (scramble species) with two different sized mung beans (large and small beans). In both sized beans, the adult emergences of each species dependen on total density of the initial larval densities of the two species and the ratio of the two densities. The emergence of one species was suppressed by the existence of the other species when the initial larval density per bean of the former species was less than that of the latter one. There were many cases in which both C. analis and C. phaseoli emerged from one bean in large beans, but such cases were quite rare in small beans. C. analis performed interference behavior only at late larval stages, whereas C. phaseoli was superior in exploitative competition all through their larval stages. These, combined with the niche segregation inside a bean, are throught to be the major factors of observed density- and frequency-dependent competition results. Based on the above experimental results, long-term competition results between the contest and scramble species were predicted.     

Bottom-up derivation of population models for competition involving multiple resources

This paper provides first-principles derivations of population models for competition involving multiple resources with different competition types, based on resource partitioning between individuals. The following two cases are investigated. The first is the case in which the resource competed for and its competition type change depending on life stages from scramble to contest competition, or from contest to scramble competition. The second is the case in which individuals compete for two resources simultaneously with scramble and contest types, respectively. In both cases, population models are derived analytically, and in particular, the Hassell model is derived in the second case. The nature of reproduction curves and the stability properties of three population models derived are compared with each other. These models provide three representative models for competition involving both scramble and contest types.     

Does heterospecific seminal fluid reduce fecundity in interspecific copulation between seed beetles?

Reproductive interference through mating between related species can cause fitness reduction and affect population dynamics of the interacting species. In experimental matings between two seed beetles, Callosobruchus chinensis and Callosobruchus maculatus, C. maculatus females, but not C. chinensis females, suffer from significant loss of fecundity when conspecific mating is followed by heterospecific mating. We hypothesized that male traits associated with sexual conflict, which are often harmful to females, pleiotropically affect fitness of heterospecific females through interspecific mating. We examined the effect of ejaculate of C. chinensis males on C. maculatus females as the cause of the fecundity loss in C. maculatus females due to interspecific copulation. We found that frequent interspecific copulation occurred between C. maculatus females and C. chinensis males, but not between C. chinensis females and C. maculatus males, resulting in frequent interspecific ejaculate transfer from C. chinensis males to C. maculatus females. However, injection of the extract from C. chinensis male reproductive organs into C. maculatus females did not significantly affect C. maculatus fecundity compared with saline injection, indicating that the effect of the heterospecific ejaculate transfer on fecundity is negligible. We suggest that other harmful male traits such as genital spines of C. chinensis males are mainly responsible for the fecundity reduction in C. maculatus females that have experienced interspecific mating.     

Contest versus scramble competition for mates: The composition and spatial structure of a population of gray mouse lemurs (Microcebus murinus) in North-west Madagascar

The modes of intrasexual competition interacting in many dispersed societies of nocturnal solitary foragers are still poorly understood. In this study we investigate the spatial structure within a free-living population of gray mouse lemurs (Microcebus murinus) in order to test for the first time the predictions from two contrasting models of male intrasexual competition on the population level. The contest competition model predicts an uneven distribution of the sexes in a population nucleus with a female biased sex ratio in the center and a male biased sex ratio in the periphery. In contrast the scramble competition model predicts males and females being distributed evenly throughout their habitat with a constant sex ratio. Nine capture/recapture periods within three consecutive mating seasons revealed a continuous male biased sex ratio in the adult population with even trapping rates for the sexes. The male biased sex ratio could either be explained with postnatal female biased mortality or with a male biased natal sex ratio. This male biased sex ratio was apparent in all parts of the study site, indicating that the population was not subdivided into a female biased core and a male biased periphery. Furthermore, the majority of adult males have been captured at the same site as or in vicinity to females. Consequently, a large proportion of males had spatial access to females during the mating season. No signs of monopolization of females by certain dominant males could be detected. These data support the predictions from the scramble competition model and the concept of a promiscuous mating system for this species.     

Ejaculate traits in relation to male body size in the eastern mosquitofish Gambusia holbrooki

In the present study, the correlation between sperm number, sperm quality (speed, viability, longevity and length), sperm bundles quality (size and dissolving rate) and male body size has been tested in the eastern mosquitofish Gambusia holbrooki a poecilid species characterized by coercive mating tactics where males do not possess obvious ornaments, and the body size is the key determinant of pre‐copulatory male mating success. The results do not tally with theoretical predictions. Indeed, no correlation between male body size and either sperm or sperm‐bundle traits has been found, evidencing the lack of the theoretically expected trade‐off between the investment in characters involved in mate acquisition and the investment in ejaculate quality. An explanation for the observed pattern comes from the extremely dynamic mating system of G. holbrooki, characterized by variable size‐related male mating success and strong post‐copulatory selective pressure, with all males facing a similar high level of sperm competition. In this situation, a higher investment in growth and maintenance at the expense of ejaculate quality is not expected. These results underscore the necessity to comprehend detailed information on species’ reproductive biology and reproductive environment to understand both the evolution of ejaculate characteristics and possible deviations from theoretical predictions.     

Sperm competition games between sneaks and guards: a comparative analysis using dimorphic male beetles

Sperm competition is widely recognized as a pervasive force of sexual selection. Theory predicts that across species increased risk of sperm competition should favor an increased expenditure on the ejaculate, a prediction for which there is much evidence. Sperm competition games have also been developed specifically for systems in which males adopt the alternative male mating tactics of sneaking copulations or guarding females. These models have not yet been tested in a comparative context, but predict that: across species male expenditure on the ejaculate should increase with increasing probability of a sneak mating; within species, sneaks should have the greater expenditure on the ejaculate; and the disparity in expenditure between sneaks and guards should be greatest in species with moderate risk of a sneak mating, and decline toward parity in species with low or high risk. Beetles in the genus Onthophagus are often characterized by dimorphic male morphologies that reflect the alternative mating tactics of sneak (minor males) and guard (major males). We conducted a comparative analysis across 16 species of male dimorphic onthophagines, finding that testes size increased across species with increasing frequency of the minor male phenotype. Minor males generally had the greater testes size, but across species the disparity between morphs was independent of the frequency of minor males. We present data on testes allometry from two populations of O. taurus that have undergone genetic divergence in the frequency of minor males. Consistent with the comparative analysis, these data support the notion that the relative frequency of sneaks in the population influences male expenditure on the ejaculate.     

Condition-dependent ejaculate size and composition in a ladybird beetle

Sexually selected male ejaculate traits are expected to depend on the resource state of males. Theory predicts that males in good condition will produce larger ejaculates, but that ejaculate composition will depend on the relative production costs of ejaculate components and the risk of sperm competition experienced by low- and high-condition males. Under some conditions, when low condition leads to poorer performance in sperm competition, males in low condition may produce ejaculates with higher sperm content relative to their total ejaculate and may even transfer more sperm than high-condition males in an absolute sense. Previous studies in insects have shown that males in good condition transfer larger ejaculates or more sperm, but it has not been clear whether increased sperm content represents a shift in allocation or simply a larger ejaculate, and thus the condition dependence of ejaculate composition has been largely untested. We examined condition dependence in ejaculate by manipulating adult male condition in a ladybird beetle (Adalia bipunctata) in which males transfer three distinct ejaculate components during mating: sperm, non-sperm ejaculate retained within the female reproductive tract, and a spermatophore capsule that females eject and ingest following mating. We found that high condition males indeed transferred larger ejaculates, potentially achieved by an increased rate of ejaculate transfer, and allocated less to sperm compared with low-condition males. Low-condition males transferred ejaculates with absolutely and proportionally more sperm. This study provides the first experimental evidence for a condition-dependent shift in ejaculate composition.