Sexual conflict does not drive reproductive isolation in experimental populations of Drosophila pseudoobscura

Sexual conflict has been predicted to drive reproductive isolation by generating arbitrary but rapid coevolutionary changes in reproductive traits among allopatric populations. A testable prediction of this proposal is that allopatric populations experiencing different levels of sexual conflict should exhibit different levels of reproductive isolation. We tested this prediction using experimentally evolved populations of the promiscuous Drosophila pseudoobscura. We manipulated sexual conflict by enforcing either monogamy, maintaining natural levels of promiscuity, or elevating promiscuity. Within each treatment, we carried out sympatric and allopatric crosses using replicated populations and examined pre-zygotic (number of mating pairs, mating speed and copulation duration) and post-zygotic (hybrid inviability and sterility) indicators of reproductive isolation. After 50 generations of selection, none of the measures conformed to predictions of sexual conflict driving reproductive isolation. Our results cannot be explained by lack of genetic variation or weak selection and suggest that sexual conflict may not be a widespread engine of speciation.     

Repeated copulations as a strategy to maximize fertilization in the fly, Dryomyza anilis (Dryomyzidae)

In the fly, Dryomyza anilis, males copulate repeatedly withthe same female during oviposition. Each copulation bout consistsof intromission followed by several tapping sequences duringwhich the male touches the external genitalia of the femalewith his claspers. The relative fertilization success of thelast male to mate with the female increases with the numberof tapping sequences. In this study, male benefits of repeatedcopulation bouts were examined by comparing matings with thesame number of tapping sequences in one and several copulationbouts. The relative fertilization success for the last maleincreased with successive copulation bouts. Simulated ovipositionpatterns showed that fertilization success in matings with manycopulation bouts was higher than in matings with one bout onlyif eggs were distributed between bouts in a certain way. Thesepredicted oviposition patterns were compared with natural ones.Although males may benefit from repeated copulation, femalesare likely to prefer matings with quick oviposition. This intersexualconflict may also affect natural oviposition patterns. It issuggested that repeated copulation in D. anilis may have evolvedin connection with males trying to secure their paternity becausefemales can discharge sperm at any moment during mating.     

Effects of multiple mating and male eye span on female reproductive output in the stalk-eyed fly, Cyrtodiopsis dalmanni

Females of the stalk-eyed fly, Cyrtodiopsis dalmanni, mate repeatedly during their lifetime and exhibit mating preferencefor males with large eye span. How these mating decisions affectfemale fitness is not fully understood. In this study, we examinedthe effects of multiple mating and male eye span on short-termreproductive output in this species. Experiments that manipulatedthe number of copulations and partners a female received suggested that obtaining a sufficient sperm supply is an important benefitassociated with multiple mating. The average percentage offertile eggs laid by females increased as a function of matingfrequency and ranged from 40% for females mated once, to 80%for females mated continuously. In addition, a high proportionof copulations in this species appeared to be unsuccessful. One-third of all females mated once laid less than 10% fertileeggs. There was no significant difference in reproductive performancebetween females mated to multiple partners and females matedto a single partner. There was also no indication that femalesreceived any short-term reproductive benefits from mating withmales with large eye span. In fact, females mated to males with short eye span laid a higher percentage of fertile eggs thanfemales mated to large eye span males.     

Sexual conflict over copula timing: a mathematical model and a test in the yellow dung fly

Sexual conflict over mating occurrence, timing, or durationis common in animals. This explains conspicuous female materejection behavior in many species, often involving shaking,fighting, and occasional forced copulations. We present a simplemodel that generates predictions about whether and when copulationoccurs in such conflict situations and how much female rejectionbehavior should be observed. Predictions depend on 2 underlyingparameters affecting female resistance and male persistence.We supply 2 qualitative tests of the model using the yellowdung fly Scathophaga stercoraria (Diptera: Scathophagidae).We manipulated adult age, body size (large and small), and adultfood availability (low and high), independently in males andfemales, staging replicate pairings of all treatment combinations.In agreement with predictions of our model, shaking durationfirst increased to a maximum at intermediate age, when the averagefemale copulated, and then decreased again. Contrary to expectation,body size did not affect copulation timing, female resistance,or male persistence. As predicted, adult food limitation delayedsexual maturity and hence prolonged female resistance, resultingin later copulations after more shaking. However, although foodlimitation equally delayed the increase in male persistencewith age, copulation also occurred later after more shaking,opposite to the model prediction. We conclude that shaking isdriven primarily by female age and male responses to it. Althoughfemale shaking can initially successfully deter males in S.stercoraria, this behavior is subtle and has apparently shiftedfunction from an effective means of mate choice to a signalof nonreceptivity, though its importance in nature remains unclear.     

The energetic cost of mating in a promiscuous cephalopod

Costs that individuals incur through mating can play an important role in understanding the evolution of life histories and senescence, particularly in promiscuous species. Copulation costs, ranging from energy expenditure to reduced longevity, are widely studied in insects but have received substantially less attention in other taxa. One cost of mating, the energetic cost, is poorly studied across all taxa despite its potential importance for the many species where copulation is physically demanding and/or frequent. Here, we investigated the energetic cost of mating in both male and female dumpling squid (Euprymna tasmanica). In this species, copulation can last up to 3 h and requires that the male physically restrains the female. We report that the act of copulation halves the swimming endurance of both sexes, and that they take up to 30 min to recover. Such a reduction in post-copulatory performance may have important implications for predator avoidance, foraging ability and energy allocation. Therefore, quantifying this cost is essential to understand the evolution of reproductive strategies and behaviours such as female receptivity and male and female mating frequency.     

Sperm competition and diversity in rodent copulatory behaviour

The copulatory behaviour of male mammals is characterized by striking diversity in patterns of copulatory stimulation and ejaculation frequency. We conducted comparative analyses of rodents to investigate the potential influence of sperm competition in the evolution of copulatory behaviour. We found that increasing sperm competition is associated with faster rates of stimulation and earlier ejaculation among species in which males perform multiple intromissions prior to ejaculation, but with no overall change in the number of intromissions per ejaculation. Increasing sperm competition is also associated with a higher frequency of repeated ejaculations with the same female, and with shorter refractory periods between repeated copulations. Increasing sperm competition level thus appears to select for male ability to ejaculate more rapidly and more frequently with each female mated. As prolonged copulations are known to reduce female remating rates, these findings indicate that males may experience opposing selection pressures on copulatory behaviour with respect to offensive and defensive aspects of sperm competition. We conclude that sperm competition is likely to be an important selection pressure explaining diversity in mammalian copulatory behaviour.     

Independent effects of familiarity and mating preferences for ornamental traits on mating decisions in guppies

The avoidance of familiar individuals as mates can act to maximizethe benefits of polyandry or might help to minimize inbreedingin small or highly philopatric populations. As previous matesare also familiar, the effects of familiarity and mating historycan often be confounded. Here, we disentangle these effectson mating decisions in the guppy, Poecilia reticulata, and examinetheir influence on sexual selection. In 3 experiments, malesand females were 1) able to mate, 2) had visual and olfactorycontact, or 3) had visual contact only. Familiarity was successfullyacquired via visual cues, and females were in all cases morelikely to mate with unfamiliar than with familiar males, indicatingthat familiarity is a more important determinant of mating outcomethan mating history. Males did not court unfamiliar femalesany more than familiar females and did not differentially allocatesperm. Familiarity did not alter the strength of sexual selectionon male coloration: we found overall positive selection forbright, large males. Female preferences for unfamiliar malesand ornamental traits may therefore be largely independent.     

Conflict of interest between sexes over cooperation: a supergame on egg carrying and mating in a coreid bug

In the golden egg bug (Phyllomorpha laciniata Vill. Heteroptera: Coreidae) females lay eggs on the backs of conspecifics, oftenon courting males. Although the bugs do not provide care tothe eggs, this decreases the risk of egg predation. As an effectmales carry many eggs which are not their own. The male andfemale interests are in conflict; females need to find an ovipositionsite, and male fitness depends on the obtained number of matings. By using a very rare modeling approach, a supergame where theindividuals actions change payoffs over time, we show thatcombinations of reciprocating strategies where males obtaina mating in return for a carried egg can be stable. The valueof the mating, to males, is more important than the relatednessto the eggs in gaining their cooperation in carrying eggs. Females may also take advantage of the males without reciprocating.This is especially likely if the probability of future meetingis high and the value of a mating is high for the male. Werelate our results to our own data from empirical studies andexperiments on the species. In the light of the results we discuss the behavior of the bugs in relation to nuptial gifts. We alsodiscuss the general applicability of the supergame approach.     

The effect of female mating history on sperm precedence in the two-spot ladybird, Adalia bipunctata (Coleoptera, Coccinellidae)

Effects of two different mating regimes on sperm precedencein the two-spot ladybird, Adalia bipunctata, were studied usingthe polymorphic gene for melanism as a marker for paternity.Virgin nonmelanic females (homozygous recessive) were matedto nonmelanic male(s) and then, after laying fertilized eggs,were mated to a melanic male of known genotype. The resultsafter the two successive single matings showed a highly variabledegree of paternity of the second male. Initial multiple matingwith nonmelanic males did not alter the pattern of paternityafter the subsequent single mating with a melanic male, butit had two other effects: (1) the female showed an increasein rejection behavior, and (2) a longer copulation was requiredfor high success of the melanic male. Additional observationsin which families were reared from beetles collected in copulain the field demonstrated that sperm competition also occursunder natural conditions. The outcome of the competition wasvariable with frequent sperm mixing.     

The costs of copulating in the dung fly Sepsis cynipsea

Finding, assessing, rejecting, and copulating with a mate isassumed to carry fitness costs, particularly for females, thathave to be traded off against fitness benefits of mating suchas increased fecundity, fertility, longevity, or better qualityoffspring. Female dung flies, Sepsis cynipsea (Diptera: Sepsidae),typically attempt to dislodge mounted males harassing themby vigorous shaking. Shaking duration has been shown to reflect both direct and indirect female choice in this species. Thelatter is an expression of the females' general reluctanceto mate due to presumed costs of mating. We investigated thecosts of copulation in the laboratory. Females were randomlyassigned to one of three treatment groups and allowed to copulateeither not at all, once, or twice. The males' armored genitalia injured females internally during copula. Injuries were visibleas sclerotized scars in the female ovipositor, and their occurrenceincreased with mating frequency. Presumably due to these injuries,mated females showed higher mortality. This effect was statisticallyindependent from additional costs of reproduction related tooviposition, as copulation also increased lifetime egg productionand tended to augment oviposition rate (eggs per day), while fertility (proportion of offspring emerged) was unaffected.We thus found high mortality costs of copulating, indicatingsubstantial sexual conflict, which helps explain female reluctanceto mate in this species.     

Control of reproduction and a survival cost to mating in female Bicyclus anynana butterflies

Abstract.  1. Given that sexual conflict is all pervasive, investigating potential costs to mating and the control of female reproduction are important issues.
2. Here, female reproductive output and longevity are investigated in relation to mating status (virgin vs. once-mated females) and host-plant availability in the tropical butterfly Bicyclus anynana .
3. Both factors significantly affected realised fecundity in a manner demonstrating that female reproduction is not entirely under control of the female herself, but is rather subject to additive contributions of the female, her male partner, and intrinsic physiological processes. As evident from the deposition of significant egg numbers by virgin, host-deprived females, B. anynana is effectively unable to completely inhibit oogenesis.
4. Mated females suffered a reduction in adult life span, which cannot be explained as a side-effect of variation in egg size, lifetime, or early fecundity.
5. Such detrimental effects of mating per se are indicative of the cooperation–conflict balance between sexes being shifted towards conflict in B. anynana .     

Influence of previous mating experience on future mating success in maleLucilia cuprina (Diptera: Calliphoridae)

Receptive and virginL. cuprina females were placed with a virgin male and an experienced male that had mated between one and five times previously. The experienced males secured significantly more matings than virgin males. Males with previous matings also gained experience in competing with males. Males directed mating attempts at each other, seemingly in the context of intrasexual competition. Experienced males directed more mating attempts at virgin males than vice versa. As their number of previous matings increased, experienced males made the first mating attempt at females more often and directed more mating attempts at females compared with virgin males. Females did not actively discriminate against experienced males, even though the proportion of matings secured on the first attempt by experienced males declined with increasing mating experience. Alternative behavioral explanations are discussed.     

Male perch selection and the mating system of the robber fly,Promachus albifacies (Diptera: Asilidae)

We studied the activity and spatial distribution of the robber fly,Promachus albifacies, in a desert grassland habitat in central New Mexico. Late in the season males spent most of the daytime on or near cholla and yucca plants that had dead stems or dead flower stalks at least 1 m high. Of the three hypotheses (thermoregulation, foraging, mate encounter site) considered as explanations for this distribution, the mate-encounter-site hypothesis was best supported. Plants used by females as oviposition sites were the focus of male activity. Males perched within or near these plants and attempted copulations with females detected nearby. Most matings were initiated at these locations. Seasonal changes in male and female activity also supported the mate-encounter-site hypothesis. Early in the season, females spent little time ovipositing, and predictably, males spent little time on or near these plants. Such a mating system may be described as resource defense polygyny, since males acted aggressively toward one another at oviposition sites even when females were not present. However, the short tenure of males at these sites is suggestive of scramble competition polygyny. We discuss possible reasons why this particular mating system has evolved.     

Lekking, resource defense, and harassment in two subspecies of lechwe antelope

For lek-breeding in ungulate populations to continue, benefitsto males defending lek territories and to females visiting leksmust outweigh the costs. In this study, Kafue lechwe males onleks gained higher mating rates than nonlekking males, a resultof sexually receptive females leaving herds and aggregatingon leks. When the numbers of females on leks were experimentallyreduced, benefits to males decreased, resulting in males graduallyabandoning lek territories. A comparison with a population ofnonlekking, resource-defending black lechwe showed that matingattempts by estrous females in herds were disrupted by harassingmales eight times more frequently in a population of lek-breedingKafue lechwe than in the nonlekking black lechwe. Despite thefact that there were fewer Kafue lechwe females on single territories,harassment of estrous females by males was greater on singleterritories of Kafue lechwe than on leks and greater than onblack lechwe resource territories. Females were also absenton Kafue lechwe single territories for long periods becauseof erratic, widespread movements of compact herds resultingfrom unpredictable distributions of resources. In contrast,black lechwe females were more evenly dispersed over homogeneousresources and for a given territory, females were likely tobe present most of the time. Therefore, unlike black lechwe,male Kafue lechwe find it uneconomical to defend resource territories.Thus, costs to estrous females mating off leks and the absenceof benefits to males attempting to defend resource-based territoriesmay be important cofactors in the appearance of lek-breedingin some ungulate populations     

A model of sexual selection and female use of refuge in a coercive mating system

In many non-monogamous systems, males invest less in progeny than do females. This leaves males with higher potential rates of reproduction, and a likelihood of sexual conflict, including, in some systems, coercive matings. If coercive matings are costly, the best female strategy may be to avoid male interaction. We present a model that demonstrates female movement in response to male harassment as a mechanism to lower the costs associated with male coercion, and the effect that female movement has on selection in males for male harassment. We found that, when females can move from a habitat patch to a refuge to which males do not have access, there may be a selection for either high, or low harassment male phenotype, or both, depending on the relationship between the harassment level of male types in the population and a threshold level of male harassment. This threshold harassment level depends on the relative number of males and females in the population, and the relative resource values of the habitat; the threshold increases as the sex ratio favours females, and decreases with the value of the refuge patch or total population. Our model predicts that selection will favour the harassment level that lies closest to this threshold level of harassment, and differing harassment levels will coexist within the population only if they lie on the opposite sides of the threshold harassment. Our model is consistent with empirical results suggesting that an intermediate harassment level provides maximum reproductive fitness to males when females are mobile.     

Dynamic games and field experiments examining intra- and intersexual conflict: explaining counterintuitive mating behavior in a Mediterranean wrasse, Symphodus ocellatus

Intersexual conflict and intrasexual competition are widelyrecognized as playing critical roles in determining mating systems.Although they occur simultaneously in populations, these processesare usually treated independently. In reality, the fitness ofreproductive strategies will depend on the outcome of both within-and between-sex conflicts. Using a modeling approach based onmultiple, linked, dynamic state variable models, we examined thereproductive behavior of a Mediterranean wrasse, Symphodus ocellatus.We compared the predictions of models that examine only a singleconflict interaction with those that consider multiple within-and between-sex conflicts simultaneously. The observed distributionof sneaker males and females among nests was compared with thosepredicted by the models. We found that the closest fit withempirical observations and experiments is given by the modelthat examines conflict between females, sneakers, and nestingmales simultaneously. Removal of successful nests indicatedthat females join nests with few or no sneakers present, whereassneakers join these nests only later, even though this leadsto lower sneaker mating success. This behavior can be explainedby observing that although sneakers would have higher fitnessat nests where the spawning rate is greater, females would notbe willing to spawn at these nests in the presence of sneakers. Presumably,once the nests have achieved high past success, females are willingto spawn in the presence of sneakers because of the associated decreasedchance of nesting male desertion.     

The effects of copulation duration in the bruchid beetle Callosobruchus maculatus

Control over copulation duration is a potentially importantgenerator of sexual conflict that has received little empiricalattention. The copulatory behavior of the bruchid beetle Callosobruchusmaculatus may reflect a sexual conflict over copulation duration.Males have spines on their intromittent organs that puncturethe female reproductive tract, and females kick their matesduring copulation. If females are prevented from kicking, copulationslast longer and the injuries females sustain are more severe.Males supposedly use the spines as anchors to prolong copulationduration, and females kick to terminate copulations. We manipulatedcopulation duration experimentally and quantified its effectson male and female fitness components to test whether or notthere is a conflict over copulation duration in C. maculatus.Females did not suffer from long copulations but instead experiencedincreased lifetime fecundity. Ejaculate size increased withcopulation duration, and females apparently derive materialbenefits from the ejaculates. Males that mated first and hadlong copulations were relatively unsuccessful when competingwith sperm from other males. However, there was a trend forfemale remating propensity to decrease with long copulationdurations, and first males may therefore also benefit from longcopulations. The copulation duration of the second male to matedid not have a significant effect on sperm precedence. We concludethat even though it seems likely that the male spines have evolvedto act as an anchor during copulation, there seems to be littleconflict over copulation duration per se in C. maculatus.     

The costs of avoiding matings in the dung fly Sepsis cynipsea

Mating is generally assumed to carry costs, particularly forfemales, which have to be traded off against each other andagainst the fitness benefits of mating. To understand any particularmating system and the evolution of sexual conflict, these costshave to be evaluated. Female dung flies, Sepsis cynipsea (Diptera:Sepsidae), typically attempt to dislodge mounted males by vigorousshaking. Such female reluctance to mate can only evolve if thecost of avoiding matings does not exceed the cost of copulation.We investigated female precopulatory costs of assessing andrejecting males in terms of increased predation, wing injuries,and (indirectly) energetics, all ultimately affecting mortality,and compared them to the costs of copulation assessed in thisand a companion study. Females housed with a male had lowersurvivorship than females housed with another female. This waslargely due to the costs of copulation rather than presumedenergetic costs of avoiding males, which were minor. Male harassmentaugmented female wing injuries, which accumulate with age inthe field and laboratory, but in laboratory experiments usingone common predator, wing injuries did not increase the susceptibilityof S. cynipsea to predation, nor did their mating behavior perse. Instead, predation was highest and survivorship lowestin all-male groups, probably because males are more activein search of females and harass each other. Overall, the precopulatorycosts of mate assessment and rejection were low relative tothe costs of copulating, explaining female reluctance behaviorin this and possibly other species.     

Accessory gland size influences time to sexual maturity and mating frequency in the stalk-eyed fly, Cyrtodiopsis dalmanni

Age at first reproduction is an extremely important life-historytrait. Several factors such as nutritional state and age-specificfecundity have been shown to influence time to sexual maturity;however, little work has been done in insects. We addressedthis in a stalk-eyed fly (Cyrtodiopsis dalmanni), by testingthe hypothesis that time to sexual maturity is associated withthe development of male internal reproductive structures. Wefound that sexual maturity was attained after an increased rateof growth in the accessory glands, several days after maturesperm bundles, and motile sperm were observed in the testes.Although testis development is essential, the results suggestthat accessory gland growth is more closely associated withthe time taken to reach sexual maturity than is testis growth.When we manipulated the growth of testes and accessory glandsvia a dietary manipulation, we found that delayed growth ratesincreased the time taken to reach sexual maturity. Among thedelayed individuals, sexually mature males had larger accessoryglands, but not testes, than did immature males. In adult males,mating frequency was significantly positively correlated withaccessory gland size, but not with testis length or body size.We conclude that accessory gland size is a critical determinantof sexual maturity and male mating frequency in this species.     

An experimental test of frequency-dependent selection on male mating strategy in the field

We provide field-based experimental evidence for the frequency-dependent nature of the fitness of alternative mating strategies. We manipulated the frequency of genetically determined phenotypic strategies in six wild populations of the side-blotched lizard, Uta stansburiana. The within-population pattern of mating was assessed using nine microsatellite loci to assign paternity. Within populations of the side-blotched lizard exist three colour morphs (orange, blue and yellow) associated with male mating strategy. The frequency of these morphs has previously been found to oscillate over a 4- to 5-year period. We found, as predicted, that the common phenotype lost fitness to its antagonist. The mating patterns of all six populations adhered to a priori predictions that were derived from previous empirical and theoretical observations on this system. We found that the frequency-dependent nature of male fitness could be accounted for by the composition of their competitors at a small local population level, driven by associations within a focal female's social neighbourhood.