Microsatellite analysis of female mating behaviour in lek-breeding sage grouse

We used microsatellite DNA markers to genotype chicks in 10 broods of lek-breeding sage grouse, Centrocercus urophasianus, whose mothers' behaviour was studied by radio-tracking and observing leks. Previous behavioural studies suggested that almost all matings are performed by territorial males on leks and that multiple mating is rare. Two broods (20%) were sired by more than one male. Genetic analyses of the broods of eight females that visited an intensively studied lek were consistent with behavioural observations. Four females observed mating produced singly sired broods and males other than the individual observed copulating were excluded as sires for most or all of their chicks. Territorial males at the study lek were excluded as sires of broods of four other females that visited the lek but were not observed mating there. Radio-tracking suggested that two of these females mated at other leks. Our results confirm the reliability of mating observations at leks, but do not rule out a possible unseen component of the mating system.     

Low levels of relatedness on black grouse leks despite male philopatry

In lekking species, males cluster on specific areas for display (the leks) and females generally prefer to copulate with males on large aggregations. The maintenance of leks in which only a few males reproduce might be explained if subordinate males gain indirect fitness benefits. By joining a lek on which relatives are displaying, subordinates might attract more females to the lek thereby increasing the mating opportunities of their kin. In black grouse, a genetic structure among leks has previously been found suggesting that relatives could display together. Using 11 microsatellite loci, we extended this result by testing for the presence of kin structures in nine black grouse leks (101 males). The genetic differentiation among flocks was higher in males than in females, suggesting female-biased dispersal and male philopatry. Because of this genetic structure, males were more related within than among leks. However, the mean relatedness within each lek hardly differed from zero. The lekking males were not more related than random assortments of males from the winter flocks and there were no kin clusters within leks. Thus, black grouse males do not choose to display with and close to relatives. Male philopatry alone was not sufficient to induce elevated levels of relatedness on the leks either because of male partial dispersal or a rapid turnover of the successful males. The indirect fitness benefits associated with males' settlement decision are probably limited compared to the direct benefits of joining large aggregations such as increased current and future mating opportunities.     

Active formation of mixed-species grouse leks: a role for predation in lek evolution?

Behavioural ecologists have interpreted avian leks as products of sexual selection, in which males display socially to increase their opportunities to mate. However, without invoking reproductive queuing or kin selection, this paradigm does not necessarily explain why many males that fail to mate participate in leks. An alternative solution, that males also aggregate to reduce predation, has previously lacked compelling support. We show that mixed-species leks, comprising two congeneric grouse, form when single males or small groups of one species, the greater prairie chicken Tympanuchus cupido, join leks of another, the sharp-tailed grouse T. phasianellus. We documented the process by observing lek dynamics and comparing group sizes between mixed- and single-species leks. Joining implies that prairie chickens benefit from displaying with sharp-tailed grouse. The numbers of females of each species attending a lek increased with the number of conspecific, but not heterospecific, males. This suggests that the joining of heterospecifics is unlikely to increase mating opportunities, and leaves lowered predation risk as the most likely benefit of associating with heterospecifics. Active formation of mixed-species leks therefore suggests that predation may be sufficient to drive lek formation. The benefits of participation in mixed leks may be asymmetrical because prairie chickens display more and are less vigilant than sharp-tailed grouse.     

Microsatellite DNA analysis shows that greater sage grouse leks are not kin groups

The spectacular social courtship displays of lekking birds are thought to evolve via sexual selection, but this view does not easily explain the participation of many males that apparently fail to mate. One of several proposed solutions to this 'lek skew paradox' is that kin selection favours low-ranking males joining leks to increase the fitness of closely related breeders. We investigated the potential for kin selection to operate in leks of the greater sage grouse, Centrocercus urophasianus, by estimating relatedness between lekking males using microsatellite DNA markers. We also calibrated these estimates using data from known families. Mean relatedness within leks was statistically indistinguishable from zero. We also found no evidence for local clustering of kin during lek display, although males tended to range closer to kin when off the lek. These results make kin selection an unlikely solution to the lek skew paradox in sage grouse. Together with other recent studies, they also raise the question of why kin selection apparently promotes social courtship in some lekking species, but not in others.     

Responses of Male and Female Black Grouse to Male Vocal Display

The evolution of leks may be explained by several hypotheses. The ‘female preference’ hypothesis, which states that females favour males that have aggregated, has recently gained some empirical support. Low-quality, unattractive males may, however, settle near attractive males, as predicted by the ‘hotshot’ hypothesis. We tested whether black grouse Tetrao tetrix females use auditory cues to find the preferred leks, and whether males respond to vocal display emitted on leks. We conducted a playback experiment with male vocal display (rookooing) on leks, where the visiting females and displaying males were counted. The number of males tended to increase more on playback leks. Specifically, the number of 1-year-old males was greater on playback sites than on control sites. Also, the number of females, in relation to the lek size before the start of the experiment tended to increase. In addition, we used aviary playback trials to test whether females distinguish between single-male and multi-male displays. In a choice test, females showed greater preference for the ‘multi-male’ tape. The tendency for increased male numbers on playback leks resulted from increased visits of young, mobile males which were attracted to leks that they perceived to be large. This suggests a ‘hotshot’-type mechanism in the settlement of young males. Because females also responded to the supplemented auditory advertisement, or directly to the increased number of males, the ‘female preference’ hypothesis is also supported. Females may, at least in part, base their decision of which lek to visit on auditory cues, but visual contact to males may be also needed.     

The anatomy of population change in a black grouse population 1992–2008

We interrogate an 18-year-long dataset containing counts of displaying male black grouse Tetrao tetrix and incidental counts of females within an 800-km² region of Perthshire, Scotland. We examine the trends in the population and investigate how different components of the population might act as signposts of different stages of overall population change. We found statistical evidence for a decline in black grouse numbers between 1992 and 2000, and then a recovery from 2002 to 2008, but little evidence for a link between population change and weather during the decline phase. There was some evidence for a positive relationship between male and female counts. The two main components of male population size, lek size and lek frequency followed the overall population trend while it was increasing, but during the earlier decline, the two became uncoupled, to expose a complex structure within the data. During the decline, when black grouse numbers were approaching their minimum, mean lek size was actually increasing. Small leks lost proportionally more birds than did large leks, and lek longevity was positively correlated with lek size, indicating that maintenance of large leks is crucial in buffering the population against serious declines. During the decline, the spatial arrangement of leks changed, with remnant leks showing tight clustering at larger spatial scales, before expanding out to fill the large areas of unoccupied landscape during the population increase. We discuss these findings in terms of species monitoring and suggest that counts of young males may add much useful demographic information with little extra effort.     

The costs of female choice in a lekking bird

We investigated the costs of active female choice in sage grouse,Centrocercus urophasianus, a lekking species in which femalesmake repeated, lengthy visits to leks to assess males beforemating. Several potential costs were measured by monitoringchanges in hens' ranging behavior, time budgets, and encounterrates with predators when they visited leks. Two costs wereidentified: hens moved further per day and encountered goldeneagles, Aquila chrysaetos, more frequently when visiting leks.However, extra travel due to visiting leks increased predicteddaily energetic expenditure by only about 1%, and the risk ofpredation by golden eagles over a typical series of lek visits(compared to a single short visit for mating) was estimatedto reduce annual survival by <0.1%. Two other potential costswere not supported: visiting leks did not depress foraging timeor conflict with nest defense. These results indicate that anycosts of mate choice are slight and imply that even very smallbenefits could be sufficient to maintain female choice. We presentcalculations which suggest that increased offspring viabilitydue to choosing fitter males could balance predation costs evenif the heritability of fitness is low and if females identifyfitter males with only moderate accuracy. Despite recent emphasison the direct benefits of mate choice, we conclude that eitherindirect or direct benefits could provide a plausible solutionto the lek paradox.     

Testing predictions for the evolution of lekking in the sandfly, Lutzomyia longipalpis

We carried out a combination of field and laboratory experiments to investigate two possible mechanisms promoting the evolution of lekking in the sandfly, Lutzomyia longipalpis. Males in this species lek on or near hosts that females visit to mate and feed. To test whether the distribution of resources, lek size and female number were positively correlated (a prediction of hotspot models) we manipulated the availability of potential lek sites by varying the numbers of chickens, Gallus gallus domesticus, held in field cages. We then investigated the distribution of males and females across leks formed within these cages and measured males to assess the relationship between male size and lek size. The number of males attracted to a lek increased with the number of hosts present and on average males on larger leks had longer abdomens. The number of females was positively correlated with the number of males present, but the average number of females per male decreased with increasing lek size. In a second experiment, we introduced single females to laboratory leks of different sizes, and compared female latency to mate. Contrary to an explicit prediction of the black hole model, lek size had a direct effect on a female's latency to mate. Females at larger leks encountered and copulated with males sooner than those at smaller aggregations, but the length of time a pair spent courting did not vary with lek size. Our results suggest that the black hole model is unlikely to explain the evolution of lekking in this species. The data instead support the hotspot model as a possible mechanism promoting lekking in L. longipalpis but suggest that female preference for larger leks may need to be invoked to obtain the degree of aggregation observed.     

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.     

Lek fidelity and movement among leks by male Greater Sage‐grouse Centrocercus urophasianus: a capture‐mark‐recapture approach

Males in lek mating systems tend to exhibit high fidelity to breeding leks despite substantial evidence of skewed mating success among males. Although movements between leks are often reported to be rare, such movements provide a mechanism for an individual to improve lifetime fitness in response to heterogeneity in reproductive conditions. Additionally, estimates of apparent movements among leks are potentially biased due to unaccounted variation in detection probability across time and space. We monitored breeding male Greater Sage‐grouse Centrocercus urophasianus on 13 leks in eastern Nevada over a 10‐year period, and estimated movement rates among leks using capture‐mark‐recapture methods. We expected that male movement rates among leks would be low, despite predictions of low breeding success for most males, and that detection rates would be highly variable among leks and years. We used a robust design multistate analysis in Program mark to estimate probability of movements among leks, while accounting for imperfect detection of males. Male Sage‐grouse were extremely faithful to their leks; the annual probability of a male moving away from its original lek of capture was approximately 3% (se = 0.01). Detection probabilities varied substantially among leks (range = 0.21–0.95), and among years (range = 0.30–0.76), but remained relatively constant within years at each lek. These results suggest that male Sage‐grouse dispersal is either rare, or consists primarily of dispersal of sub‐adults from their natal areas prior to the breeding season. The study highlights the benefits of robust design multistate models over standard ‘live‐encounter’ analyses, as they not only permit estimation of additional parameters, such as movement rates, but also allow for more precise parameter estimates that are less sensitive to heterogeneity in detection rates. Additionally, as these data were collected using capture‐mark‐recapture methods, our approach to estimating movement rates would be beneficial in systems where radiotagging is detrimental to the study organism.     

Indirect Effects of an Existing Wind Energy Facility on Lekking Behavior of Greater Prairie‐Chickens

Rapid expansion of the wind energy industry has raised concerns about the potential effects of anthropogenic disturbance on prairie grouse. While efforts have been made to address the effects of wind energy facilities on measures of fitness, their effect on the behaviors of prairie grouse has been largely neglected. To address these concerns, we investigated the effects of an existing wind energy facility in Nebraska that became operational in 2005 on the lekking behavior of male greater prairie‐chickens Tympanuchus cupido pinnatus between March and May 2013. Given the potential for disturbance caused by wind turbine noise to disrupt acoustic communication and thus behavior, we predicted that males at leks close to, compared to far from, the wind energy facility would spend more time in agonistic behaviors, and less in booming displays. Given the potential for wind turbine noise to reduce the number of females attending leks (hereafter ‘female lek attendance’), we also predicted that males at leks close to the wind energy facility would spend more time in non‐breeding behaviors and less time in breeding behaviors than males farther from the facility. Although we found no effect of the wind energy facility on female lek attendance, males at leks closer to the wind energy facility spent less time in non‐breeding behaviors than those at leks farther away. However, distance from the wind energy facility had no effect on time spent performing booming displays, flutter jumps, or in agonistic behaviors. Given that lekking behaviors of males influence mating success, our results may have consequences for the fitness of prairie grouse breeding in the vicinity of wind energy facilities.     

Female mate choice across spatial scales: influence of lek and male attributes on mating success of blue-crowned manakins

Lekking males compete for females within and among leks, yet female choice is expected to work differently at each of these spatial scales. We used paternity analyses to examine how lek versus male attributes influence mate choice in the blue-crowned manakin Lepidothrix coronata. We tested the hypotheses that females prefer (i) to mate at larger leks where a larger number of potential mates can be assessed, (ii) to mate with unrelated or highly heterozygous males expected to produce high-quality offspring, (iii) to mate with males that display at higher rates, and that (iv) display honestly reflects male genetic quality. Our results show that (i) males at larger leks are not more likely to sire young, although females nesting close to small leks travel further to reach larger leks, (ii) siring males are not less related to females or more heterozygous than expected, (iii) within a lek, high-display males are more likely to sire young, and (iv) both male heterozygosity and display rate increased with lek size, and as a result display does not reliably reflect male genetic quality across leks. We suggest that female mate choice in this species is probably driven by a Fisherian process rather than adaptive genetic benefits.     

Restrictive mating by females on black grouse leks

In bird species with pair bonds, extra-pair matings could allow females to choose genetically superior males. This is not needed in lekking species because female choice is not constrained by pairing opportunities. However, polyandry has been reported in most lekking species studied so far. Using 12 microsatellite loci, we determined the paternity of 135 broods of black grouse sampled between 2001 and 2005 (970 hatchlings and 811 adult birds genotyped). The paternity assignments were combined to lek observations to investigate the mating behaviour of black grouse females. About 10% of the matings seemed to take place with males displaying solitarily. Forty per cent of the copulations between males displaying on the studied leks and radio-tagged females were not recorded. This was due to difficulties in identifying the females and because our observations did not cover all the possible time for matings. However, females of the undetected copulations had chosen males that were already known to be successful on the leks. There was a strong consistency between the observations and true paternity, even when the copulation was disturbed by a neighbouring male. Multiple mating and multiple paternities were rare. We can now confidently ascertain that most females mate only once with one male for the whole clutch. This mating behaviour requires that a single insemination is sufficient to fertilize a clutch and that females can determine whether the sperm has been successfully transferred. Grouse Tetraoninae with many lekking species may be the only bird taxon that has evolved these traits.     

Assessing lek attendance of male greater sage-grouse using fine-resolution GPS data: Implications for population monitoring of lek mating grouse

Counts of males displaying on breeding grounds are the primary management tool used to assess population trends in lekking grouse species. Despite the importance of male lek attendance (i.e., proportion of males on leks available for detection) influencing lek counts, patterns of within season and between season variability in attendance rates are not well understood. We used high-frequency global positioning system (GPS) telemetry data from male greater sage-grouse (Centrocercus urophasianus; n = 67) over five lekking seasons (2013–2017) at eight study sites in Nevada to estimate lek attendance rates. Specifically, we recorded daily locations of sage-grouse in relation to mapped lek boundaries and used generalized additive models to assess temporal variation in attendance rates by age class (subadult vs. adult). Average timing of peak attendance occurred on 16 April but varied from March 16, 2014 to April 21 , 2016. Overall, adult males attended leks at higher rates (0.683 at peak) and earlier in the season (19 March) than subadults (0.421 at peak on April 19). Peak attendance probability was positively related to cumulative winter precipitation. Daily probabilities of lek switching differed between adults (0.019 at peak on March 3) and subadults (0.046 at peak on March 22), and lek switching was negatively related to distance to nearest lek. Our results indicate variable patterns in lek attendance through time, and that lek switching may occur at higher rates than previously thought. We demonstrate the use of generalizable daily attendance curves to date-correct lek counts and derive estimates of male abundance, although such an approach will likely require the incorporation of information on age structure to produce robust results that are useful for population monitoring.     

Combs and sexual selection in black grouse (Tetrao tetrix)

We studied supra-orbital combs in lekking black grouse (Tetrao tetrix) in relation to sexual selection at five leks in Finland1991-1998 and four leks in Sweden 1992-1995. Comb size wasestimated in two ways: by observing its natural size in thefield at different behaviors ("observed comb size"), and bymeasuring the comb size from captured birds ("measured combsize"). The size of combs is highly variable, and individualscan change it within seconds. Males express their larger combsduring display, as compared to other behaviors. Observed mean comb sizes were larger on leks with a higher number of malesand a higher number of copulations. Measured and observed combsizes and copulatory success did not significantly correlatewhen all males where analyzed, but a positive and significantrelationship between observed comb size and copulatory success was found within males that achieved copulations. Measured comblength correlated positively with the amount of testosterone.While females were present on the lek, displaying and successfulmales showed the largest observed comb size. When we comparedobserved comb size during fighting between successful and unsuccessfulmales and correlated comb size of pairs of fighting males withtheir fighting activity, no significant differences in combsize were found. The result that comb size correlated significantlywith an increase in testosterone level and that larger combsize, within successful males, predicted higher copulatorysuccess suggests that combs may be a cue for females to assessmale quality. The lack of a significant relationship betweenobserved comb size and fighting behavior suggests that combsize either has minor importance in male-male signaling onthe lek or that males may express similar-sized combs duringfighting to avoid serious fights and thus risk of comb injuries.     

Lek formation by female choice: a simulation study

We used computer simulation to study the formation of matingaggregations under the influence of female choice. Female movementswere not constrained by home range size. Males formed clumpeddispersions if females expressed strong preferences either forlarger leks or for male quality. High travel costs for femalesvisiting leks produced male dispersions that matched the initialdistribution of females. High costs to females for waiting formatings produced evenly dispersed males. Depending on the relativeweights of these factors, a continuous range of outcomes froma single lek per population to evenly dispersed males was produced.The results suggest that effects of female choice on lek evolutionare more likely to be detected by studying the processes bywhich leks form than by characterizing the spatial distributionof displaying males.     

Dynamic Disturbance Processes Create Dynamic Lek Site Selection in a Prairie Grouse

It is well understood that landscape processes can affect habitat selection patterns, movements, and species persistence. These selection patterns may be altered or even eliminated as a result of changes in disturbance regimes and a concomitant management focus on uniform, moderate disturbance across landscapes. To assess how restored landscape heterogeneity influences habitat selection patterns, we examined 21 years (1991, 1993–2012) of Greater Prairie-Chicken (Tympanuchus cupido) lek location data in tallgrass prairie with restored fire and grazing processes. Our study took place at The Nature Conservancy’s Tallgrass Prairie Preserve located at the southern extent of Flint Hills in northeastern Oklahoma. We specifically addressed stability of lek locations in the context of the fire-grazing interaction, and the environmental factors influencing lek locations. We found that lek locations were dynamic in a landscape with interacting fire and grazing. While previous conservation efforts have treated leks as stable with high site fidelity in static landscapes, a majority of lek locations in our study (i.e., 65%) moved by nearly one kilometer on an annual basis in this dynamic setting. Lek sites were in elevated areas with low tree cover and low road density. Additionally, lek site selection was influenced by an interaction of fire and patch edge, indicating that in recently burned patches, leks were located near patch edges. These results suggest that dynamic and interactive processes such as fire and grazing that restore heterogeneity to grasslands do influence habitat selection patterns in prairie grouse, a phenomenon that is likely to apply throughout the Greater Prairie-Chicken’s distribution when dynamic processes are restored. As conservation moves toward restoring dynamic historic disturbance patterns, it will be important that siting and planning of anthropogenic structures (e.g., wind energy, oil and gas) and management plans not view lek locations as static points, but rather as sites that shift around the landscape in response to shifting vegetation structure. Acknowledging shifting lek locations in these landscapes will help ensure conservation efforts are successful by targeting the appropriate areas for protection and management.     

Mate choice in lekking sage grouse revisited: the roles of vocal display, female site fidelity, and copying

In lekking sage grouse (Centrocercus urophasianus), femalesexhibit relatively unanimous mate choice for particular males,but a satisfactory explanation for this unanimity has been elusive.We present analyses of mating distributions from two leks over4 years that provide evidence for female choice based on differencesin vocal display performance of males, the locations at whichhens mated in the previous year, and the choices of other females(copying). The unanimity of female choice varied markedly amongleks and years in correlation with changes in the mean numbersof hens that mated at the same time and hence the opportunityto copy. The results confirm that hens assess phenotypic traitsof males directly but also indicate that the secondary tacticsof site fidelity and copying are often important componentsof female choice. The occurrence of these secondary tacticshas three implications: the variance in mating success amonglek males will be a poor predictor of the intensity of sexualselection on specific traits; female preferences may generatemore clustered dispersions of displaying males than predictedby hotspot settlement models; and direct assessment of malesby females may be difficult or costly, a conclusion that supportsadaptive models of sexual selection over a nonadaptive Fisherianprocess. [Behav Ecol 1991;2:165–180]     

Habitat Manipulation Modifies Lek Use in Fallow Deer

Fallow deer leks and single territories often persist in specific locations over many years. In our study area in Tuscany, one site (Lek 1) was used as a lek by fallow deer for at least 30 years. Females passed through the lek year-round while travelling between sheltering and foraging sites. In 1987–89, forestry operations affected areas near the lek that were used by females as travel routes, but the lek site itself was not affected. After the logging operations, very few females traversed the lek site. Over the next 2 years the lek decreased in size (both in terms of number of territories defended and number of territorial males) until it became a single territory, and after two more years it was abandoned. Another lek (Lek 2) whose access routes were unaffected by forest cuts, continued to exist. Territorial males abandoned Lek 1 and moved to Lek 2 when female visits to Lek 1 became rare. Our results suggest that female movement patterns can be affected by habitat manipulations, and that females will not return to traditional mating sites that become external to their home ranges. Male fallow deer may form leks along female movement routes, where they experience a high female encounter rate as predicted by the hotspot model.     

Both habitat change and local lek structure influence patterns of spatial loss and recovery in a black grouse population

Land use change is a major driver of declines in wildlife populations. Where human economic or recreational interests and wildlife share landscapes this problem is exacerbated. Changes in UK black grouse Tetrao tetrix populations are thought to have been strongly influenced by upland land use change. In a long-studied population within Perthshire, lek persistence is positively correlated with lek size, and remaining leks clustered most strongly within the landscape when the population is lowest, suggesting that there may be a demographic and/or spatial context to the reaction of the population to habitat changes. Hierarchical cluster analysis of lek locations revealed that patterns of lek occupancy when the population was declining were different to those during the later recovery period. Response curves from lek-habitat models developed using MaxEnt for periods with a declining population, low population, and recovering population were consistent across years for most habitat measures. We found evidence linking lek persistence with habitat quality changes and more leks which appeared between 1994 and 2008 were in improving habitat than those which disappeared during the same period. Generalised additive models identified changes in woodland and starting lek size as being important indicators of lek survival between declining and low/recovery periods. There may also have been a role for local densities in explaining recovery since the population low point. Persistence of black grouse leks was influenced by habitat, but changes in this alone did not fully account for black grouse declines. Even when surrounded by good quality habitat, leks can be susceptible to extirpation due to isolation.