Queuing in space and time reduces the lek paradox on an antelope lek

Lek systems, where females often use centrality to assess male quality, highlight a general paradox in evolutionary biology: how can female preferences for males providing good genes persist when consequential strong directional selection is predicted to deplete additive genetic variance in male quality and thereby obliterate benefits of choosiness? An explanation contributing to the resolution of this lek paradox may be that genetic variance is retained when an indirect mate choice cue, such as centrality on a lek, is an imperfect indicator of male genetic quality. Here I investigate whether the presence of alternative male mating tactics limits the reliability of centrality as a quality indicator in lek-breeding topi antelopes. Whereas males establishing territories directly on the central lek were relatively large, smaller peripheral males regularly shifted their territories centripetally and in this way also occasionally obtained central territories. By such opportunistic queuing, small males could increase their mating success drastically; however, their territorial tenure in the lek centre was relatively short, consistent with moderate competitive ability. These results suggest that male topi antelopes can obtain central lek territories through alternative mating tactics, providing scope for variance in male quality on the central lek. In a separate finding, the mating success of central males was found to increase during territorial tenure, independent of estimated age. The demonstration of queuing in both space and time on a mammalian lek highlights the importance of considering male tactical dynamics over time in order to avoid an inflated appearance of the lek paradox.     

Physiological costs enforce the honesty of lek display in the black grouse (Tetrao tetrix)

Females may use condition-dependent sexual traits as reliable cues of male “quality” if the costs of the expression of such traits vary with male “quality”, and if there is positive genetic correlation between male traits and condition. However, there are multiple ways of measuring the changes in body condition which reflect physiological costs meaning that the multifaceted nature of the physiological costs associated with the expression of sexual traits has rarely been thoroughly examined. In the lekking black grouse (Tetrao tetrix), mating success is highly skewed towards males defending central territories and having high survival rates to the following year, but the mechanisms underpinning such superior performance remain unclear. In this study, we quantified the changes in five measures of body condition before and after the mating season and related these changes to male lek performance (fighting rate, territory centrality and mating success) to understand the physiological costs of male reproductive effort. Between the two capture sessions, male body mass decreased significantly, blood parasite counts and plasma carotenoid concentration increased substantially while the total immunoglobulin concentration tended to increase. There was no overall impairment of individual body condition as the changes in the five measures of body condition were unrelated. Male fighting rate was unrelated to changes in the condition measures but males losing more body mass defended central territories and had high mating success. Therefore, females preferring central, dominant males may select males better able to afford the energetic costs of lek performance thereby effectively enforcing the honesty of male display.     

Correlates of male mating success and female choice in a lek-breeding antelope

We investigated factors underlying variation in male matingsuccess in Uganda kob (Kobus kob thomasi), a lek-breeding antelope.We found that only heavy (and, possibly, relatively old) malesheld lek territories and that female choice was an importantdeterminant of nonrandom mating patterns at leks. Our measureof male mating success was closely related to the historicalpopularity of the territory that a male defended, and individualfemales showed consistent preferences for particular lek territories,despite changes in territory ownership. Male success increasedwith body weight and declined independently of territory effectsduring each bout of lek territory tenure. We also found someevidence that female kob copied one another's choice of matesbecause females arriving at a lek tended to join territoriesthat already had relatively large harems on them. When comparedacross leks, average male mating success increased with leksize. Our results suggest that female kob may use a suite ofmale- and territory-based cues in mate choice at leks and, asa result, mate with particularly large males. However, we wereunable to determine whether female kob gain any direct or indirectbenefits through mate choice at leks.     

Mating strategies of topi bulls: getting in the centre of attention

In lek-breeding ungulates, only some males defend clustered lek territories, and others defend dispersed territories or are nonterritorial. In this study of lekking topi antelopes, Damaliscus lunatus, we measured male mating benefits directly by observing matings and investigated why the alternative mating strategies coexist. A multivariate analysis showed that proximity to the lek centre had an overriding, positive, effect on male mating rate. With increasing distance to the lek centre, proximity of a territory to a drainage line became increasingly important in enhancing male mating success. On the other hand, costs of lekking were suggested by higher hyaena density on leks, relatively poor body condition of lek males, and more frequent agonistic encounters, with central lek males more likely to sustain bleeding wounds than others. Probably as a consequence of the intense competition for central lek territories, males defending such territories were larger than others and, judging from horn wear, they were also older than resource defenders. Not only did males defending central lek territories achieve the highest instantaneous mating rate and resource defenders the lowest, but the same order was also likely for overall lifetime reproductive success when we took territorial tenure into account. These results suggest that male mating strategies are phenotype limited, as demands on male quality increase with proximity to the lek centre. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

To lek or not to lek: mating strategies of male fallow deer

We studied the mating system of fallow deer (Dama dama) for6 years in central Italy. Males in this population could defendterritories that were either single, clumped in leks, or satelliteto leks. The most highly successful males in our study werein leks. When we considered all males, there were no significantdifferences in average copulatory success according to territorytype because many lek males did not achieve any copulations,which were seen in only a few lek territories. The variancein copulatory success, however, was much greater for leks thanelsewhere. Single territories were occupied for shorter timesduring the rut than lek territories. Fighting among males wasmore frequent in the lek, even when we excluded highly successfullek males from the analysis. Chases of nonterritorial malesand harem size were correlated with the number of copulationsachieved by individual males, but did not vary according toterritory type. Copulatory success of some individuals increasedwith age, but there were no age differences among males holdingdifferent types of territories. Satellite males switched tolek territoriality in the course of one rut, but switches fromsingle territory to lek territory were rare. We suggest thatmales in single territories are inferior competitors that selecta low-risk, lowbenefit strategy, whereas those in lek territorieswhere no copulations were seen may be attempting to establishthemselves on the lek to increase their copulatory success infuture years.     

Black holes, mate retention, and the evolution of ungulate leks

In some ungulates living in unstable herds, females in estrusleave their usual groups and join males defending mating territories.During the 12-24 h before mating, females commonly move severaltimes between males. These movements are commonly caused byharems being disrupted by young males or by overenthusiasticcourtship by the territorial male. When females leave a territorythey typically move to its nearest neighbor. Under these circumstances,clusters of territories can retain estrous females until theymate and leave the lek. This paper develops a model to investigatethe benefits of defending clustered versus dispersed territoriesto males and the consequences of variation in the rate of femalemovement between territories (P_m) and the tendency for femalesto move from one territory to a neighboring territory (a). Wherefemales move between territories at least once every 24 h (P_m< 0.04) and usually move to neighboring territories (a <0.5), the mating success of males is inversely related to thedistance from their territory to its nearest neighbor, and malesdefending clustered territories have higher mating rates thanthose defending dispersed territories. This process may be importantin the initial evolution of ungulate leks, which may resembleblack holes, attracting and retaining estrous females untilthey mate and their estrus ceases. It provides one possibleexplanation of the evolution of ungulate leks that does notrely on female preferences for mating with particular phenotypiccategories of males.     

Uganda kob prefer high-visibility leks and territories

In lekking species, where males provide estrous females withlittle more than sperm, it has been widely supposed that theonly possible benefits to females of mate choice are genetic.We studied female choice of leks and territories in a reduncineantelope, the Uganda kob (Kobus kob thomasi), and found thatfemales consistently preferred high-visibility mating sites.Leks were elevated and had shorter grass and fewer thicketsthan the surrounding areas. Changes in the number of male andfemale kob on 10 leks were correlated with changes in surroundinggrass height, and both females and males preferred leks withexperimentally reduced grass height over neighboring controls.Within a lek, territory popularity was the primary determinantof male daily mating success, and females preferred territoriesrelatively far from thickets, but removal of thickets did notaffect female territory preferences. Because lion hunting successon kob increases with grass height and thicket density, femalesmay benefit directly from these preferences by reducing therisk of predation.     

Context-dependent effects of tail-ornament damage on mating success in black grouse

Male black grouse (Tetrao tetrix) may receive damage to theirtail ornaments, the lyre, during goshawk predation attemptsand during fights with other males. In this study we confirma previous observation that black grouse males with damagedtail ornaments suffer reduced mating success. In males thatheld territories on the edge of the leks, tail damage was unrelatedto mating success, whereas in central males damage was negativelycorrelated with mating success. We tested experimentally whetherabsence of damage is used by females in mate choice. In maleswith edge territories, intact, control males had higher matingsuccess than males with cut tails, but in males with centralterritories, lyre cutting had no effect on mating success. Theseresults suggest two interpretations. First, female choice alsodepends on factors other than tail damage such as position onthe lek and dominance. Second, the effect of tail damage iscontext dependent; in males that otherwise meet females standards(e.g., dominant males), the effect of tail damage is negligible,but in less dominant males, tail damage could be used by femalesin mate selection. The second interpretation provides an explanationfor why the data on unmanipulated and manipulated birds differ.In experimental central birds, factors other than tail damageprobably determine male mating success, whereas in experimentaledge birds such factors are probably absent and therefore taildamage is relatively more important. In central unmanipulatedbirds, however, males with natural damage are probably not chosenbecause tail damage and absence of other attractive traits arecorrelated. The absence of an effect on peripheral unmanipulatedbirds may be explained by their overall low mating success     

Evolution of black grouse leks: female preferences benefit males in larger leks

Leks, communal display grounds in which males display and femalesonly attend to mate, represent one of the most remarkable outcomesof sexual selection. There have been no detailed studies thatcompare the behavior of males and females between leks of differentsizes to test if there is any benefit for male clumping andto test the many hypotheses suggested to explain lekking. Inthe black grouse, Tetrao tetrix, larger leks have many morefemale visits and copulations, leading to a higher average malemating success. Females visiting larger leks are also more likelyto mate, indicating that female preferences of males are importantfor the evolution of leks. Yearling males seldom copulate, buttheir presence on the lek increases the mating success of adultmales, suggesting that lek size per se and not only male qualityaffects female preferences for larger leks. The distributionof males over lek sizes agrees with a game theory model of idealfree distribution with unequal competitors, in which less competitivemales go to smaller leks.     

Effects of Removal of Successful Males in a Fallow Deer Lek

Removal of 5 of the 8 most successful males in a fallow deer lek between breeding seasons led to an increase in fighting rate of males and a decrease in mating rate of both sexes. The increase in fighting was likely due to disruption of the social hierarchy. The lower mating rate of females was not due to disruption of copulations by territorial males, nor did it appear to result from disturbance from fights. We suggest that difficulties in mate choice related to an unstable male hierarchy resulted in females either increasing their length of stay in the lek, visiting the lek more than once before mating, or leaving the lek without mating.     

Aggression among Lekking Male Fallow Deer (Dama dama): Territory Effects and Relationship with Copulatory Success

We studied the aggressive behavior of territorial male fallow deer (Dama dama) at two leks. Daily number of escalated fights was not correlated with number of matings. A dominance index including all agonistic interactions was weakly correlated with copulatory success; the correlation was stronger when each half of the rut was considered separately. Dominance likely changed over the rut due to fatigue. We ranked lek territories by the number of copulations seen in each. Males that won fights were likely to take over the loser's territory only if it ranked higher than the one they held. Winners were more likely to fight with a third male after defeating an opponent that held a higher-ranking territory than one from a lower-ranking territory. Exposure to attacks by third-party males may be a major cost of fighting. Males appear aware of the relative value of different lek territories, but the frequency of aggression was not scaled to potential fitness benefits, possibly because males seldom fought with opponents they were unlikely to beat. The outcome of interactions on the lek may not always reflect the relative dominance rank of the contestants. Females are unlikely to use the outcome of fights as a direct criterion for mate selection.     

No peace for estrous topi cows on leks

Male coercion, such as harassment, may be considered the thirdmain component in sexual selection alongside male competitionand female choice. In this study on lek-breeding topi antelopes(Damaliscus lunatus), I investigate whether female mating preferenceshave consequences for male investment in harassment and whetherharassing males are more likely to succeed in mating. I thenaddress the question of whether lek evolution in topi can beexplained by harassment avoidance. Judging from mating rate,I found that female topi antelopes in estrus preferred lek malesto resource defenders. In contrast to lek males, resource defendersdemonstrated significantly higher harassment rates before theysucceeded in mating than when they did not, and the precopulatoryharassment rate was significantly higher on resource territoriesthan on lek territories. After mating on resource territories,harassment dropped to low levels. Thus, resource defenders,but not lek males, seem to employ harassment as a strategy tocoerce females to mate against their preference. However, byusing various measures of harassment intensity, overall estrousfemales were found to experience higher harassment levels onlek, and chases by intruders were relatively rare on all territorytypes. These findings suggest that harassment avoidance is unlikelyas an explanation for lek evolution.     

Are Centrally Displaying Males Always the Centre of Female Attention? Acoustic Display Position and Female Choice in a Lek Mating Subterranean Insect

Several conceptual models seek to explain patterns of male display and factors that influence female mate choice in lek mating systems. The central advantage model predicts that males displaying at or near the lek centre should be more attractive to females than are males positioned along the lek periphery. Females may exhibit biases toward these centrally displaying males based on either spatial or display‐related cues. We tested the prediction of the central advantage model in investigating the importance of male display position in the subterranean and lek mating prairie mole cricket (Gryllotalpa major). Gryllotalpa major males form mating aggregations in the early spring and produce an acoustic advertisement signal from a constructed calling chamber at the soil surface. Pair formation occurs in the calling chamber, and males typically maintain these structures for the duration of the reproductive season. To assess whether G. major females exhibit a preference for males calling from centrally located acoustic burrows, we documented the spatial position and number of female attractions for all advertising males across the focal lek. Six spatial attributes related to display position were reduced using principal component analysis and examined for an association with male attractiveness. We found that in general, female attractions were distributed randomly across the lek; male attractiveness was not related to proximity to the lek centre nor to any factor associated with display position. The most highly attractive males, however, were located further from the lek centre and from nearest calling neighbours than other attractive males. Advertising males that segregate themselves within the aggregation and locate nearer the lek margin may gain a geometric advantage resulting in the increased probability of attracting a searching female.     

Encounter with heavier females changes courtship and fighting efforts of male field crickets Gryllus bimaculatus (Orthoptera: Gryllidae)

The effects of mating experience on male mating behavior are mediated by four factors: mating cost, such as resource depletion, perception of mating opportunities, self-perception of attractiveness, and female quality. For example, encountering females might increase male expectations of prospective mating opportunities, while copulation increases self-perception of attractiveness in males. To determine the relative importance of these factors, the effect of mating on the two components of reproductive effort (courtship and fighting effort) in Gryllus bimaculatus was examined. Calling activity before and after encountering females was measured, and copulation success was recorded. Subsequently, the intensity and outcome of male–male fighting behavior was recorded. Female encounter increased calling activity irrespective of copulation, thereby indicating that the perception of mating opportunities is important factor for the males. Changes in courtship effort of males were larger and fighting success was lower when they were previously paired with relatively heavier females. These results indicate that male reproductive effort is also affected by quality of previous mating partners.

     

Relationships between Blood Parasites, Mating Success and Phenotypic Cues in Male Sage Grouse Centrocercus urophasianus

In lek breeding Sage Grouse Centrocercus urophasianus in easternCalifornia, male mating success is strongly correlated withindividual differences in lek attendance, and in the rate andacoustic quality of courtship display, suggesting that theseprovide cues by which females choose mates. Increased lek attendanceand high display rates are also associated with elevated metabolicexpenditure. This paper examines the hypothesis that the abilityto commit energy to display is related to the incidence of bloodparasites. A single hematozoan genus, Haemoproteus, was foundin 37.5% of 184 Sage Grouse sampled over a five year period.Parasitism varied across years and increased through the breedingseason. However, no measure of display performance or matingsuccess was significantly correlated with decreased parasiteload among adult males. Several additional lines of evidence,including numerically low infection intensities, the absenceof detectable effects of parasites on hematocrit and erythrocyteproduction, and the seasonal distribution of parasite incidenceallsuggested that infections were unlikely to impact male courtshipdisplay. Alternative factors maintaining individual variationin male display performance in this population are also evaluated.     

Uncertainty in territory quality affects the benefits of usurpation in a Mediterranean wrasse

Individuals should defend sites when the expected benefits ofthe territory exceed the cost of defense. However, if territoryqulaity is unpredictable or difficult to assess, the expectedpattern of territorial behavior is less clear. In a Mediterraneanwrasse, Symphodus ocellatus, mating success is skewed with 2%of nesting males getting more than 20% of the spawning success.Yet, variation in mating success is not explained by any knownphysical characteristic of males or their territories. Instead,females prefer nests with a recent history of mating successbecause males are less likely to desert the offspring she leavesbehind. Thus, territory quality is transient and determinedby interactions between the sexes. I measured the frequencyof territorial takeovers and the uncertainty in mating successamong days at a nest. Observations indicated that S. ocellatusmales usurped their neighbor's successful nests when males wereunsuccessful and larger than their successful neighbor. Sitesthat achieved mating success had a significantly higher probability(0.84) of remaining sucessful between consecutive days thanunsuccessful territories had of becoming successful (0.30).Unsuccessful males obtained higher and more certain fitnessreturns if they usurped a successful neighbor's territory. Interactionswithin and between the sexes drive uncertainty in success, whichinfluences territorial behavior in this species.     

How predation risk affects the temporal dynamics of avian leks: greater sage grouse versus golden eagles

Leks often attract predators as well as mates, yet most evolutionary models have assumed that sexual selection, not predation, drives lekking behavior. We explored the influence of predation on lek dynamics using a stochastic dynamic game model based on the lek-breeding greater sage grouse (Centrocercus urophasianus) and its principal avian predator, the golden eagle (Aquila chrysaetos). The model predicts time-dependent male lek attendance as a function of factors affecting both mating success (female arrival rate, male numbers, and social status) and predation risk (eagle arrival rate and group size). Dominant males are predicted to arrive sooner and leave later than subordinates, especially if mating skew is high, predation risk is low, or the relationship between lek size and female arrival rate is weak. Both high mean levels of predation risk and small lek size should reduce lek attendance, but the relative tendency of predators to attack large versus small leks has little influence on predicted lekking behavior. Field observations confirmed the predicted effects of female arrival rate, lek size, male dominance, and weather-dependent predator arrival rates on lek departure times. Predicted effects of female arrival rates and male dominance on seasonal lek attendance were also supported. Our model provides an empirically supported adaptive explanation for short-term lek dynamics. It also suggests alternative interpretations for phenomena previously invoked to support the hotshot and skew models of lek formation.     

Mate retention, harassment, and the evolution of ungulate leks

Current models of lek breeding mostly suggest that males defendclustered mating territories because females show a preferencefor mating on leks. Here we argue that, in lek-breeding ungulates,males may also gain benefits from holding clustered mating territoriesbecause clusters retain does in estrus. We show that in fallowdeer (Dama dama) harems are commonly disrupted by young males.Bucks that hold territories on the lek that lose their haremsquickly regain does as other harems are disrupted, whereas bucksdefending isolated, single territories rarely regain does thesame day. The risk of harassment may also help to explain whydoes in estrus leave the large, unstable herds that they usuallylive in. Does in estrus are frequently chased by young maleswhen outside male mating territories. Benefits of moving tothe lek (versus moving to single territories) include reducedrisks of long chases. Though intrusions by young bucks are thecommonest cause of does leaving male territories in our studypopulation, other factors that cause does to move between neighboringharems (including disturbance by predators and persistent courtshipby males) may generate benefits to males holding clustered matingterritories. Once clustered mating territories have developed,the additional costs of mate choice are likely to be low, andfemale preferences for particular male characteristics may belikely to develop.     

Male position and calling effort together influence male attractiveness in leks of the medfly,Ceratitis capitata (Diptera: Tephritidae)

Despite the close association between lek mating systems and the study of female mate choice, male mating success in leks is often associated with other aspects of sexual selection as well as female choice of male display traits. Males of the medfly Ceratitis capitata form leks on the undersides of leaves of their host plants. By experimentally creating artificial leks, we show that male success at attracting females depends not only on male calling effort (pheromone production dispersed by wing movement), but also on the position of the male within a lek. Males in the highest position in the artificial lek (closest to the light) attracted more females, and received more visits from those females. In our experiment, we deliberately minimized the visual cues that females approaching a male could use and, under these conditions, found no associations between male attractiveness and male size, weight or fluctuating asymmetry, either of the wings or sex setae (a pair of bilateral supra‐fronto‐orbital bristles). The latter result contrasts with earlier studies showing a significant negative association between sex setae fluctuating asymmetry and mating success. Accordingly, we conclude that symmetry of the male sex setae has no role in nonvisual communication (e.g. through directing pheromone plumes). Mating patterns associated with this insect are therefore every bit as complex as those in vertebrate leks. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 479–487.     

Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus

In many animals, variance in male mating success is strongly correlated with male dominance rank or some other measure of fighting ability. Studies in primates, however, have varied greatly in whether they detect a relationship between male dominance rank and mating success. This variability has led to debate about the nature of the relation between rank and mating success in male primates. We contribute to the resolution of this debate by presenting an analysis of the relationship between dominance rank and male mating success over 32 group-years in a population of wild savannah baboons. When data were pooled over the entire period, higher-ranking males had greater access to fertile females. However, when we examined successive 6-month blocks, we found variance in the extent to which rank predicted mating success. In some periods, the dominance hierarchy functioned as a queue in which males waited for mating opportunities, so that rank predicted mating success. In other periods, the queuing system broke down, and rank failed to predict mating success when many adult males were in the group, when males in the group differed greatly in age, and when the highest-ranking male maintained his rank for only short periods. The variance within this single population is similar to the variance observed between populations of baboons and between species of primates. Our long-term results provide strong support for the proposition that this variance is not an artefact of methodological differences between short-term studies, but is due to true variance in the extent to which high-ranking males are able to monopolize access to females. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.