Sexual selection and condition dependence of courtship display in three species of horned dung beetles

Sexual selection has traditionally been divided into competitionover mates and mate choice. Currently, models of sexual selectionpredict that sexual traits are expressed in proportion to thecondition of their bearer. In horned beetles, male contestcompetition is well established, but studies on female preferencesare scarce. Here I present data on male mating success and condition dependence of courtship rate in three species of horn-dimorphicdung beetles, Onthophagus taurus, Onthophagus binodis, andOnthophagus australis. I found that in the absence of malecontest competition, mating success of O. taurus and O. australiswas unrelated to their horn length and body size, whereas inO. binodis horn size had a negative effect but body size hada positive effect on male mating success. Overall, in O. binodismajor morph males had greater mating success than minor morphmales. In all three species male mating success was affectedby courtship rate, and the courtship rate was condition dependent such that when males were manipulated to be in poor conditionthey had lower courtship rates than males that were manipulatedto be in good condition. My findings provide new insight intothe mating systems of horned dung beetles and support an importantassumption in indicator models of sexual selection.     

Mating tactics in external fertilizers when sperm is limited

Among externally fertilizing animals in aquatic habitats, theproportion of a female's egg clutch that is successfully fertilizedoften falls below 100%. In many such species, particularly incoral reef fishes, males spawn daily at high frequencies, oftenwith little or no sperm competition. A major evolutionary problemfor such males is how best to allocate sperm over successivespawns. Females face the problem of ensuring complete fertilizationof their egg clutch. Here we model male and female mating tacticswhen daily sperm production is limited and with various assumptionsconcerning how differences in the number of sperm released duringa mating influence the number of eggs fertilized. The modelsreveal conditions under which males can maximize daily reproductivesuccess, either by releasing a fixed number of sperm duringall successive spawns or by matching sperm numbers to the clutchsize of their mates. These patterns of sperm allocation exertdifferent pressures on females, which may respond evolutionarilyby developing various mating tactics of their own.     

Males with short horns spent more time mating in the Japanese horned beetle Allomyrina dichotoma

We examined the relationships between male body and horn sizes and mating duration in the Japanese horned beetle, Allomyrina dichotoma. Smaller males possessing shorter horns spent more time for copulation with a female and mounting the female without copulation. The results of multiple regression analyses indicate that the horn length is a determining factor for the time spent by the males during mating. A previous study has documented that the horn length of male A. dichotoma primarily determined the outcomes of aggressive male–male interactions; hence, predicts access to females. Therefore, instead of fighting for females, males possessing short horns may maximize their fertilization success by mating longer with the few females they have access to.     

Intraspecific female brood parasitism in the dung beetle Onthophagus taurus

Abstract.  1. Brood parasitism occurs when individuals parasitise each others' investment into parental care, and has been documented primarily as an interspecific interaction. Intraspecific brood parasitism, in contrast, is often difficult to detect and quantify, and evidence for it is comparatively scarce. The present study documents the occurrence of intraspecific brood parasitism by females of the tunnelling dung beetle Onthophagus taurus , and investigates the contributions of two variables to the propensity of female brood parasitism: female body size and dung desiccation rate.
2. Female O. taurus were found to routinely utilise brood balls made by conspecific females as food provisions for their own offspring.
3. Contrary to expectations, large and small females did not differ in the likelihood of engaging in brood-parasitic behaviour.
4. Dung desiccation rate appeared to influence likelihood of brood parasitism. Females that were given access to rapidly drying dung were significantly more likely to detect and utilise brood balls produced by conspecific females.
5. While interspecific brood parasitism has been documented in dung beetles before, the present study is among the first to present evidence for intraspecific brood parasitism as an alternative reproductive tactic of female dung beetles. Results are discussed in the context of the evolutionary ecology of onthophagine beetles.     

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.     

Mating tactics and male-male courtship in the lek-breeding cichlid Oreochromis mossambicus

Data are presented on the breeding behaviour of Oreochromis mossambicus under captive conditions. Males tended to synchronize their occupation of territories and breeding activities. Different male mating tactics were observed, namely establishing a breeding territory, acting as a floater, or behaving as a sneaker. The majority of spawnings observed involved dominant males and were subjected to interference from other males. Males were found to court other males that frequently responded to these attempts by adopting a female-like behaviour. Results are discussed in terms of a probable time constraint in territoriality, which promotes male-male competition and a low level of sex discrimination by territorial fish.     

Mating Frequency, Fecundity and Fertilization Success in the Hide Beetle, Dermestes Maculatus

While the immediate benefits accrued to females through multiple mating are well documented, the effect of sperm depletion for multiply mating males is rarely considered. We show that, in small mixed-sex laboratory aggregations, both male and female hide beetles, Dermestes maculatus (De Geer) mated multiply. There was considerable variation in the mating frequency of both sexes; however the skew in mating success was comparable for males and females. Several individuals that mated multiply also re-mated with a previous partner, but in a competitive environment no male copulated more than seven times. Mating success was unrelated to an individual's size, but males that had the most inter-sexual matings also engaged in the most intra-sexual mating attempts. In a second experiment, we show that, even in the absence of rivals, only a small number of males mated with all available virgin females. Moreover, even though males were mated twice to each female, males that copulated more than eight times failed to fertilize any eggs. We suggest that under natural conditions male hide beetles may refrain from mating either prior to, or at the point of, sperm depletion thereby reducing the selection pressure for females to discriminate against sperm depleted males. However, fecundity and fertilization success varied considerably across females and even those mating with sperm-replete males were unable to fertilize 100% of their egg batch. Thus, direct fertilization benefits accrued by females through mating more than once with the same male may play a key role in the maintenance of polyandry in this species.     

The effect of a seasonal time constraint on development time, body size, condition, and morph determination in the horned beetle Allomyrina dichotoma L. (Coleoptera: Scarabaeidae)

Abstract.  1. In horned beetles selection favours males that adjust their investment in horn development in relation to cues that predict adult body size. Here it is shown that in the Japanese horned beetle, Allomyrina dichotoma . There is a significant discontinuity in the horn length body size allometry. This can be described as a linear relationship that is shifted towards an increased horn length to body length ratio in males with horns longer than 16 mm.
2. Larval nutrition explains morph determination in A. dichotoma . However, unlike other species, variation in larval nutrition was the result of a seasonal time constraint that limits the time available for feeding prior to the onset of winter diapause.
3. Even when eggs were reared with an ad libitum food supply, minor morphs were still observed. Individuals that were oviposited later in the season had less time to feed, shorter development times, eclosed as smaller individuals and, in the case of males, were more likely to be hornless. Major morphs, minor morphs, and females all reduced their body size in response to seasonal time constraints in the same way. However, males that were laid later in the season had faster development times than females laid at the same time, but showed no reduction in their size relative to females, suggesting seasonal time constraints increase growth rates in males but not in females.
4. No evidence was found that seasonal time constraints resulted in a reduction of size-corrected fat reserves at eclosion, or that minor morphs gained any developmental advantage by reducing investment in horn length.     

The effects of reproduction on courtship, fertility and longevity within and between alternative male mating tactics of the horned beetle, Onthophagus binodis

Life history theory provides a powerful tool to study an organism's biology within an evolutionary framework. The notion that males face a longevity cost of competing for and displaying to females lies at the core of sexual selection theory. Likewise, recent game theory models of the evolution of ejaculation strategies assume that males face a trade-off between expenditure on the ejaculate and expenditure on gaining additional matings. Males of the dung beetle Onthophagus binodis adopt alternative reproductive tactics in which major males fight for and help provision females, and minor males sneak copulations with females that are guarded by major males. Minor males are always subject to sperm competition, and consistent with theoretical expectation, minor males have a greater expenditure on their ejaculate than major males. We used this model system to seek evidence that mating comes at a cost for future fertility and/or male expenditure on courtship and attractiveness, and to establish whether these traits vary between alternative mating tactics. We monitored the lifespan of males exposed to females and nonmating populations, and sampled males throughout their lives to assess their fertility and courtship behaviour. We found a significant longevity cost of reproduction, but no fertility cost. On average, males from mating populations had a lower courtship rate than those from nonmating populations. This small effect, although statistically nonsignificant, was associated with significant increases in the time males required to achieve mating. Minor males had lower courtship rates than major males, and took longer to achieve mating. Although we did not measure ejaculate expenditure in this study, the correlation between lower courtship rate and longer mating speed of minor males documented here with their greater expenditure on the ejaculate found in previous studies, is consistent with game theory models of ejaculate expenditure which assume that males trade expenditure on gaining matings for expenditure on gaining fertilizations.     

Mutual mate choice by mountain pine beetles: size‐dependence but not size‐assortative mating

1. Mutual mate choice may be rare, occurring when both sexes invest heavily in reproduction, mating opportunities are abundant, and individuals differ in quality. 2. Mountain pine beetles, Dendroctonus ponderosae (Curculionidae: Scolytinae) appear to meet the conditions for mutual mate choice. We introduced males to females in breeding sites and observed the occurrence and speed of a male entering a female's gallery. We tested for consequences of mutual mate choice, namely condition‐dependent choosiness and assortative mating. 3. Males were more likely to enter a female's gallery when the gallery was in a smaller tree with less resin production and when the gallery was larger. Female body size and condition did not influence the probability of entry. Larger males were less likely to enter a gallery than were smaller males, probably because of size‐dependent choosiness rather than physical limitations. 4. Small males took longer to enter galleries of large females than of small females, whereas large males entered as quickly into galleries of large females as small females. This suggests size‐dependent choosiness by females. 5. No assortative mating by body size was detected, probably because males appeared to choose on the basis of female‐associated resources rather than on female traits.     

Insecticide resistance enhances male reproductive success in a beetle

Abstract.— Malathion-specific resistance in the red flour beetle, Tribolium castaneum , is widespread and stable in natural populations even in the absence of pesticide exposure. To understand this stability, both resistant and susceptible males were placed in competition for susceptible female fertilization. Females were then isolated and their progeny was tested for malathion susceptibility. Male reproductive success was estimated for populations originating from different geographic areas and for isogenic strains. In most cases, resistant males had a greater reproductive success rate than susceptibles. The results suggest that male reproductive success is not traded against the selection for malathion resistance, even resistant individuals are at an advantage for this fitness trait. This absence of fitness cost may be the result of postselection of (1) modifier gene which ameliorate the fitness of resistant individuals or (2) nondeleterious resistance gene. Resistant phenotype superiority could be due to increased male mating success, improved ability of resistant males in sperm competition, female mate choice, and/or cryptic female choice of resistance gene(s). The effect of male phenotypic frequency on male reproductive success was also examined. We observed that male fertilization success is frequency dependent and inversely related to their frequency. However, this "rare male" advantage did not counteract the superiority of the resistant males.     

Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits

Sperm competition is widely recognized as a potent force in evolution, influencing male behavior, morphology, and physiology. Recent game theory analyses have examined how sperm competition can influence the evolution of ejaculate expenditure by males and the morphology of sperm contained within ejaculates. Theoretical analyses rest on the assumption that there is sufficient genetic variance in traits important in sperm competition to allow evolving populations to move to the evolutionarily stable equilibrium. Moreover, patterns of genotypic variation can provide valuable insight into the nature of selection currently acting on traits. However, our knowledge of genetic variance underlying traits important in sperm competition is limited. Here we examine patterns of phenotypic and genotypic variation in four sperm competition traits in the dung beetle Onthophagus taurus. Testis weight, ejaculate volume, and copula duration were found to have high coefficients of additive genetic variation (CV(A)S), which is characteristic of fitness traits and traits subject to sexual selection. Heritabilities were high, and there was some evidence for Y-linked inheritance in testis weight. In contrast, sperm length had a low CV(A), which is characteristic of traits subject to stabilizing selection. Nevertheless, there was little residual variance so that the heritability of sperm length exceeded 1.0. Such a pattern is consistent with Y-linked inheritance in sperm length. Interestingly, we found that testis weight and sperm length were genetically correlated with heritable male condition. This finding holds important implications for potential indirect benefits associated with the evolution of polyandry.     

Mating unplugged: a model for the evolution of mating plug (dis-)placement

Mating plugs are male-derived structures that may impede female remating by physically obstructing the female genital tract. Although mating plugs exist in many taxa, the forces shaping their evolution are poorly understood. A male can clearly benefit if his mating plug secures his paternity. It is unclear, however, how plug efficacy can be maintained over evolutionary time in the face of counteracting selection on males' ability to remove any plugs placed by their rivals. Here, I present a game-theory model and a simulation model to address this problem. The models predict that evolutionarily stable levels of mating-plug efficacy should be high when (1) the number of mating attempts per female is low; (2) the sex ratio is male-biased, and (3) males are sperm-limited. I discuss these results in the light of empirical data.     

Male body size and condition affects sperm number and production rates in mosquitofish,Gambusia holbrooki

Sperm number is an important predictor of paternity when there is sperm competition. Sperm number is often measured as maximum sperm reserves, but in species where mating is frequent, males will often be replenishing their reserves. Thus, variation in how quickly males can produce sperm is likely to be important in determining male success in sperm competition. Despite this, little is known about how male size, body condition or diet affects sperm production rates. We counted sperm number in large and small Gambusia holbrooki (eastern mosquitofish) after 3 weeks on either a high or low food diet. Sperm number was significantly higher in both larger males and in well‐fed males. We then stripped ejaculates again either 1, 2, 3, 4 or 5 days later to investigate subsequent sperm production. The rate of sperm replenishment was influenced by an interaction between size and diet. Large, well‐fed males had consistently high levels of sperm available over the 5 days (i.e. rapid replenishment), whereas small poorly fed males showed consistently low levels of sperm availability over the 5 days (i.e. slow replenishment). In contrast, large, poorly fed and small, well‐fed males increased their sperm numbers over the first 3 days (i.e. intermediate replenishment). Our study highlights that when mating is frequent and sperm competition is high, size and condition dependence of maximal sperm number and of sperm production rate might both contribute to variation in male reproductive success.     

Sperm investment and alternative mating tactics in bluegill sunfish (Lepomis macrochirus)

Although alternative mating tactics are found in males of manyspecies, little is known about tactic-specific adaptations tosperm competition and the mechanism by which fertilization successis obtained. We now report on the sperm investment patternsof males that use alternative mating tactics in bluegill sunfish(Lepomis macrochirus). Bluegill males are characterized by threealternative mating tactics: parentals, sneakers, and satellites.Parentals delay maturation and adopt a courting and guardingtactic, whereas sneakers and satellites mature precociouslyand, respectively, use sneaking and female mimicry to stealfertilizations from parentals. We found differences among thetactics in testes weight, sperm longevity, and ejaculate spermdensity and competitiveness. Parentals had the largest testes,but the smallest relative to their body weight. Satellites hadintermediate-sized testes, and sneakers had the smallest testes,but the largest relative to their body weight. Within each tactic,there was a positive relationship between testes weight andbody weight, but the exact relationship differed among the tacticsand could not be attributed solely to allometry. Parentals hadlonger-lived sperm compared with that of both sneakers and satellites.Ejaculate sperm density was greatest in sneakers, satelliteswere intermediate, and parentals had the lowest. Competitionexperiments involving equal volumes of ejaculate showed thatfertilization success increased linearly with sperm number,consistent with a rafflelike process. However, independent ofsperm number, parental sperm were superior at fertilizing eggs.We interpret these sperm investment patterns in relation todifferences in sperm competition risk, number of mating opportunities,and alternative investment options.     

Mating refusal and its significance in females of the ladybird beetle, Harmonia axyridis

ABSTRACT. . Mating receptivity in females of the ladybird, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), was studied with reference to internal and environmental conditions. Females sometimes reject copulation: they run away, or shake off the male and bend the abdomen upwards. Newly emerged females show a greater likelihood of accepting copulation with an advance in the stage of ovarian development, this being related to age. Females usually mate repeatedly, but frequently show refusal behaviour under unfavourable food conditions. Dissections reveal that females which accept copulation have a greater number of mature eggs in the ovary than do rejectors. Results also suggest that the food conditions are a major environmental factor, directly controlling mating receptivity.     

Role of Contests in the Scramble Competition Mating System of a Leaf Beetle

Male competition for mates can occur through contests or a scramble to locate females. We examined the significance of contests for mates in the leaf beetle Chrysomela aeneicollis, which experiences a short breeding season. During peak mating season, 18–52% of beetles are found in male-female pairs, and nearly half of these are copulating. Sex ratios do not differ from parity, females are larger than males, and positive size-assortative mating occurs. Males fight (2–4% of beetles) over access to females, and disruption of mating usually follows these contests. In the laboratory, we compared mating and fighting frequencies for males found in mating pairs (field-paired) and single males placed into an arena with a field-paired female. Mating pairs were switched in half of arenas (new male-female pairs) and maintained in the other half. For 2 days, each male was free to move about and fight; thereafter males were tethered to prevent contests. Mating frequencies were significantly greater for field-paired than single males in both situations. Male size was not related to mating frequency; however, large females received more matings than small ones. These data suggest that males fight for high quality females, but otherwise search for as many matings as possible.     

Correlates of reproductive success within alternative mating tactics of the common shrew

Male common shrews (Sorex araneus) adopt two discrete matingtactics. The most successful males, in terms of number of offspringfathered, are those that establish large overlapping home rangesin areas of high female density early in the breeding season.An alternative, less successful mating tactic is to travel longdistances in search of mating opportunities. This study is aninvestigation of correlates of reproductive success for malesadopting these different mating tactics. Reproductive successunder natural conditions was assessed using DNA fingerprinting,and survival of offspring was monitored in the field. The numberof offspring fathered by males with overlapping home rangeswas positively correlated with the number of female ranges overlappedduring the breeding season and with testes mass. The numberof offspring fathered by males that made long-distance movementswas positively correlated with their epididymal sperm counts.It is argued that competitively superior (overlapping) malesachieve high reproductive success by competing to maximize thenumber of females inseminated, whereas those adopting an alternativemating tactic instead compete largely via sperm competition,aiming to maximize insemination success with any particularfemale. There was no significant difference in the fluctuatingasymmetry (FA) of males adopting different mating tactics (FAwas measured as the difference in length of the paired lateralscent glands). Fluctuating asymmetry was not related to thenumber of offspring fathered by males adopting either matingtactic, but was significantly correlated with the proportionof male offspring fathered that survived to sexual maturity.Although apparently not correlated with mating success in thisspecies, FA may reflect some aspect of genetic quality thataffects offspring survival. [Behav Ecol 7: 334–340 (1996)]     

Reproductive apparatus and male accessory structures in two batrachoid species (Teleostei, Batrachoididae)

The morphology of the genital apparatus of two batrachoid species, Opsanus tau and Porichthys notatus , was studied. The anatomical organization of the female reproductive apparatus is similar in both species but differences are observed in the rhythm of gametogenesis with individual oocyte production asynchronous in O. tau and group synchronous in P. notatus. The male reproductive apparatus is similarly organized in the two species, with both showing enlongated testes with an efferent duct system, two main testicular ducts, a common sperm duct, and a pair of multi-channel accessory structures. The sperm transport system consisting of the efferent duct system, main testicular ducts, and sperm duct is more developed in P. notatus and only in this species does it secrete sialoglycoproteins. Male accessory organs also secrete sialoglycoprotein in both species, but they appear more developed in O. tau. Intraspecific variability in development of accessory structures and mucin secretion was also observed between the two male morphs of P. notatus. Type I males, which build nests and perform parental care to eggs and fry, have larger accessory organs and more abundant secretion than type II males, which adopt opportunistic spawning tactics. The possible role played by mucins as components of the seminal fluid, in both species, and their inter-and intraspecific variability are discussed in the light of the reproductive biology and the presence of alternative male mating tactics.