Christophe Lebigre

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.

Female‐biased dispersal alone can reduce the occurrence of inbreeding in black grouse (Tetrao tetrix)

Although inbreeding depression and mechanisms for kin recognition have been described in natural bird populations, inbreeding avoidance through mate choice has rarely been reported suggesting that sex‐biased dispersal is the main mechanism reducing the risks of inbreeding. However, a full understanding of the effect of dispersal on the occurrence of inbred matings requires estimating the inbreeding risks prior to dispersal. Combining pairwise relatedness measures and kinship assignments, we investigated in black grouse whether the observed occurrence of inbred matings was explained by active kin discrimination or by female‐biased dispersal. In this large continuous population, copulations between close relatives were rare. As female mate choice was random for relatedness, females with more relatives in the local flock tended to mate with genetically more similar males. To quantify the initial risks of inbreeding, we measured the relatedness to the males of females captured in their parental flock and virtually translocated female hatchlings in their parental and to more distant flocks. These tests indicated that dispersal decreased the likelihood of mating with relatives and that philopatric females had higher inbreeding risks than the actual breeding females. As females do not discriminate against relatives, the few inbred matings were probably due to the variance in female dispersal propensity and dispersal distance. Our results support the view that kin discrimination mate choice is of little value if dispersal effectively reduces the risks of inbreeding.

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.

EXTRA-PAIR PATERNITY AND THE VARIANCE IN MALE FITNESS IN SONG SPARROWS (MELOSPIZA MELODIA)

The variance in fitness across population members can influence major evolutionary processes. In socially monogamous but genetically polygynandrous species, extra‐pair paternity (EPP) is widely hypothesized to increase the variance in male fitness compared to that arising given the socially monogamous mating system. This hypothesis has not been definitively tested because comprehensive data describing males’ apparent (social) and realized (genetic) fitness have been lacking. We used 16 years of comprehensive social and genetic paternity data for an entire free‐living song sparrow (Melospiza melodia) population to quantify and compare variances in male apparent and realized fitness, and to quantify the contribution of the variances in within‐pair reproductive success (WPRS) and extra‐pair reproductive success (EPRS) and their covariance to the variance in realized fitness. Overall, EPP increased the variance in male fitness by only 0–27% across different fitness and variance measures. This relatively small effect reflected the presence of socially unpaired males with zero apparent and low realized fitness, small covariance between WPRS and EPRS, and large variance in WPRS that was relatively unaffected by EPP. Therefore, although EPP altered individual males’ contributions to future generations, its impact on population‐level parameters such as the opportunity for selection and effective population size was limited.

Leucocyte counts variation and measures of male fitness in the lekking Black Grouse

Differences in the ability to sustain chronic stress can underlie the variation in individuals’ fitness directly or indirectly by impairing the expression of condition-dependent signals used in female mate choice. Therefore, understanding the effect of the stress response on individuals’ fitness is key to identifying the mechanism of sexual selection. We tested the hypothesis that an indicator of stress—the heterophil/lymphocyte ratio (H/L ratio)—is related to several major components of male fitness in the lekking Black Grouse (Tetrao tetrix), a species with intense male–male competition. The H/L ratio accurately measured the stress response, as it increased within a few hours of trapping and during the months prior to the mating season. The H/L ratio was positively related to the expression of morphological traits, suggesting that males of higher “quality” might be able to express elaborated ornaments and better cope with stressful conditions or with changes in health status. However, in Black Grouse, ornaments are (partly) independent of behavioural display and are under only weak selective pressure. Therefore, the H/L ratio was not significantly related to male mating success and survival to the following year. Under natural conditions, observed levels of the H/L ratio might not be associated with strongly deleterious effects because of behavioural adjustments. Mechanisms other than the stress response may mediate the observed variance in male mating success.ZusammenfassungDie Fähigkeit, chronischen Stress auszuhalten, kann den Schwankungen individueller Fitness direkt oder indirekt zugrunde liegen, durch die Beeinträchtigung der Expression konditionsabhängiger Signale, die bei der Weibchenwahl eine Rolle spielen. Daher ist das Verständnis des Effekts der Stressreaktion auf die individuelle Fitness entscheidend, um die Mechanismen zu identifizieren, durch die sexuelle Selektion wirken kann. Wir haben die Hypothese getestet, dass ein Stressanzeiger—das Heterophile/Lymphozyten-Verhältnis (H/L-Verhältnis)—mit mehreren Hauptkomponenten der Fitness von Männchen des im Lek balzenden Birkhuhns (Tetrao tetrix), einer Art mit intensiver Männchenkonkurrenz, in Zusammenhang steht. Das H/L-Verhältnis maß akkurat die Stressreaktion, da es innerhalb weniger Stunden nach dem Fang und in den Monaten vor der Paarungszeit anstieg. Das H/L-Verhältnis stand in positiver Beziehung zu der Expression morphologischer Merkmale, was darauf hindeutet, dass Männchen höherer “Qualität” in der Lage sein könnten, aufwändige Ornamente auszubilden und besser mit Stressbedingungen oder Veränderungen ihres Gesundheitszustands fertig zu werden. Bei Birkhühnern sind Ornamente jedoch (teilweise) unabhängig von Balzverhalten und unterliegen nur schwachem Selektionsdruck. Daher stand das H/L-Verhältnis in keinem signifikanten Bezug zum Paarungserfolg der Männchen und ihrem Überleben bis zum nächsten Jahr. Es könnte sein, dass die beobachteten H/L-Verhältnisse unter natürlichen Bedingungen keine starken schädlichen Wirkungen haben, da Verhaltensanpassungen erfolgen. Andere Mechanismen als die Stressreaktion könnten die beobachtete Varianz im männlichen Fortpflanzungserfolg herbeiführen.

Life-history differences in age-dependent expressions of multiple ornaments and behaviors in a lekking bird.

Age is a major factor explaining variation in life-history traits among individuals with typical patterns of increasing trait values early in life, maximum trait expression, and senescence. However, age-dependent variation in the expressions of sexually selected traits has received less attention, although such variation underpins differences in male competitive abilities and female preference, which are central to sexual selection. In contrast to previous studies focusing on single traits, we used repeated measures of seven sexually selected morphological and behavioral traits in male black grouse (Tetrao tetrix) to quantify the effects of age and life span on their expressions and quantified this variation in relation to male reproductive effort. Trait expression increased with age, but long-lived males had a slower increase and delayed maxima in trait values compared with short-lived males. There was evidence of terminal investment (increasing trait values during the last breeding season) in some traits and senescence in all traits. These trait dynamics were largely explained by the timing of male peak lekking effort. This study shows that fully understanding the variation in sexually selected traits and fitness benefits associated with sexual selection requires accounting for the complex interaction among individual age, life span, and the timing of individuals’ investment in reproduction.

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.

Age-dependent inbreeding risk and offspring fitness costs in female black grouse

Dispersal is an important mechanism used to avoid inbreeding. However, dispersal may only be effective for part of an individuals lifespan since, post-dispersal individuals that breed over multiple reproductive events may risk mating with kin of the philopatric sex as they age. We tested this hypothesis in black grouse Tetrao tetrix, and show that yearling females never mated with close relatives whereas older females did. However, matings were not with direct kin suggesting that short-distance dispersal to sites containing kin and subsequent overlap of reproductive lifespans between males and females were causing this pattern. Chick mass was lower when kinship was high, suggesting important fitness costs associated with inbred matings. This study shows that increased inbreeding risk might be a widespread yet rarely considered cost of ageing.

Restrictive mate choice criteria cause age-specific inbreeding in female black grouse, Tetrao tetrix

Inbreeding is generally rare in large, natural populations yet mate choice often appears to be random with respect to kinship. This suggests that the risks of inbreeding may be small because passive mechanisms of inbreeding avoidance, for example dispersal, are effective at lowering inbreeding risk. Previous theoretical and empirical studies have assumed that the risks of inbreeding are constant over an individual’s life span, but in the lek-breeding black grouse, inbreeding increases with female age. To determine whether inbreeding avoidance mechanisms are also age dependent, we generated four null models of random mate choice ranging from complete randomness to more biologically realistic mate choice criteria and compared these to 8 years of data on inbreeding levels at four different female age classes. We additionally tested whether mate fidelity decreased inbreeding risk. Observed inbreeding in female age classes 1, 2 or <3 were not significantly different from random, but was approximately 3.5 times higher in female age class <4. Alternative models using mate choice criteria showed no significant differences between observed and expected levels for any age class. Our results are in line with previous studies on noncooperatively breeding passerine birds, which indicate that mating is random with respect to kinship and that increased inbreeding in older females can be explained by reduced male availability caused by restrictive mate choice criteria. We also found that individuals that switched mates significantly increased relatedness to partners suggesting that mate fidelity may have evolved as an important passive inbreeding avoidance mechanism.

Flexible timing of reproductive effort as an alternative mating tactic in black grouse ( Lyrurus tetrix ) males

Alternative reproductive tactics often take the form of dichotomous behavioural phenotypes. Focusing attention on such obvious dichotomy means that flexible patterns of behaviour within tactics is largely ignored. Using a long-term dataset of black grouse (Lyrurus tetrix) lek behaviours, we tested whether there were fine-scale differences in reproductive effort (lek attendance, fighting rates) and whether these were related to age and phenotype. Yearling males increased their lek attendance and fighting rate to a peak when adult male effort was declining. Adults and yearlings allocated reproductive effort according to their body mass but this was unrelated to differences in timing of effort. In adult males, different patterns of lek attendance were associated with different costs of reproduction, measured by mass loss or gain. Overall, our work demonstrates that individuals can use flexible patterns of reproductive effort both in terms of their own condition, their age and the likely costs of behaviours.