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.

Limited indirect fitness benefits of male group membership in a lekking species.

In group living species, individuals may gain the indirect fitness benefits characterizing kin selection when groups contain close relatives. However, tests of kin selection have primarily focused on cooperatively breeding and eusocial species, whereas its importance in other forms of group living remains to be fully understood. Lekking is a form of grouping where males display on small aggregated territories, which females then visit to mate. As females prefer larger aggregations, territorial males might gain indirect fitness benefits if their presence increases the fitness of close relatives. Previous studies have tested specific predictions of kin selection models using measures such as group-level relatedness. However, a full understanding of the contribution of kin selection in the evolution of group living requires estimating individuals' indirect fitness benefits across multiple sites and years. Using behavioural and genetic data from the black grouse (Tetrao tetrix), we show that the indirect fitness benefits of group membership were very small because newcomers joined leks containing few close relatives who had limited mating success. Males' indirect fitness benefits were higher in yearlings during increasing population density but marginally changed the variation in male mating success. Kin selection acting through increasing group size is therefore unlikely to contribute substantially to the evolution and maintenance of lekking in this black grouse population.

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 individual's 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.

Reduced dispersal propensity in the wingless waterstrider Aquarius najas in a highly fragmented landscape.

Dispersal behaviour of animals in fragmented habitats has generated intensive theoretical attention but empirical data on the evolution of dispersal are still relatively scarce. Theory predicts reduced dispersal propensity in small and isolated habitat patches. We tested these predictions in the waterstrider Aquarius najas, a wingless species with special habitat demands. Flightlessness constrains insect dispersal and as a stream specialist A. najas cannot survive on still water. Lakes therefore represent a dispersal barrier for this species. We measured dispersal propensity of the waterstrider A. najas which originated from ten fragmented populations. In the experiment, we transplanted laboratory-grown individuals to the field. We did not find differences between sex in dispersal propensity. However, we found that waterstriders that originated from small and isolated patches moved less than individuals from large and more continuous habitats. This suggests that the cost of dispersal over hostile surrounding habitats may be high. We conclude that a low likelihood of dispersal in A. najas is an adaptation to small and isolated stream habitats.

Signal reliability compromised by genotype-by-environment interaction and potential mechanisms for its preservation.

Sexual selection based on signaling requires that signals used by females in mate choice are reliable indicators of a male's heritable total fitness. A signal and the preference for it are expected to be heritable, resulting in the maintenance of genetic covariance between these two traits. However, a recent article has proposed that signals may quickly become unreliable in the presence of both environmental variation and genotype-by-environment interaction (G x E) with crossing reaction norms, potentially compromising the mechanisms of sexual selection. Here we examine the heritability and plasticity of a male dominance advertisement in the bank vole, Clethrionomys glareolus, in stable and changing rearing environments from father to son. The bank vole is naturally exposed to considerable sources of spatial and temporal environmental variation and male reproductive success is determined by both intra- (male-male competition) and inter- (females prefer to mate with dominant males) sexual selection. Significant G x E for male dominance was found with crossing reaction norms. Plasma testosterone level (T), rather than condition, determined a male's dominance and T also showed a significant G x E. Dominance showed a considerable plasticity across environments, but was only heritable under stable conditions. We document a negative between-environments correlation of male dominance, suggesting that when the environment changes between father and son, the dominance signal is unreliable to females and sexual selection may be compromised. We discuss how G x E and environmental variation interacting with other mechanisms may preserve the reliability of signals and thus the mechanism of sexual selection itself.

Color signals in the black grouse (Tetrao tetrix): signal properties and their condition dependency.

Recent progress in techniques of quantifying between-individual differences of color-based ornaments has revealed undiscovered possibilities for research in sexual selection. We present how the color spectra data can be comprehensively used for studying the importance of sexual ornaments in the black grouse and how these ornaments are related to a male condition. For this, we used both correlative field and experimental data. Field data indicated that older males had more chromatic coloration than yearlings. Blue chroma of males was correlated with male mating success. We experimentally manipulated yearling birds with testosterone implants and found that testosterone-implanted males had impaired expression of several sexual ornaments: 10 months after the implantation, both structural-based blue and carotenoid-based red eye comb coloration were diminished, as well as lyre (tail) length. However, the manipulation did not affect vital traits under natural selection (wing length or body mass). Our data indicate that structural color is an important trait in sexual selection in this lekking species. Importantly, the data also indicate that male sexual ornaments are more susceptible to environmental conditions than the other male traits, thus showing their heightened condition dependency compared with the other traits mediating the honesty of signaling.

Maternal antibodies in a wild altricial bird: effects on offspring immunity, growth and survival.

1. In many animals immunity is not fully developed until adulthood but the young still need protection against various sets of pathogens. Thus, bird nestlings are highly dependent on antibodies received from their mother (in the eggs) during their rapid early growth period. The relationship between maternal immunity and the development of neonates' own immunity has been poorly studied. 2. It has been suggested that immune function plays an important part in mediating resource competition between different life-history traits, e.g. growth and reproduction. Maternal investment of antibodies has potentially permanent effects on offspring phenotype. Thus, the trade-offs between the immune function and other important life-history traits in the offspring will also affect the fitness of the mother. 3. Our supplemental feeding experiment in the magpie Pica pica indicates that the immunoglobulin levels of offspring at hatching are dependent on a mother's nutritional condition. In addition, the amount of maternal immunoglobulins transferred to offspring increases along the laying order within a nest. 4. We also found that at the age of 8-10 days the immunoglobulin production of the offspring has already begun. Furthermore, the maternal immunoglobulin levels of the offspring at hatching were positively related to their immunoglobulin levels on day 10. 5. Maternal immunoglobulins did not significantly affect offspring growth, but there was a negative relationship between self-produced immunoglobulins and growth over the first 10 days, indicating a trade-off between these traits. Nestlings' weight, however, had a positive relationship with immunoglobulin production suggesting that the observed trade-off between growth and immunoglobulin production is due to catch-up growth of nestlings with a low hatching weight. We found that within nests nestlings with higher maternal antibody levels had higher survival rate until day 20, but between nests there was an opposite relationship. 6. Evidently, there is a trade-off, in magpies, between maternal resources, immune function and growth, shaping the evolution of maternal investment in offspring immunity.

Short- and long-term population dynamical consequences of asymmetric climate change in black grouse.

Temporal asymmetry in patterns of regional climate change may jeopardize the match between the proximate and ultimate cues of the timing of breeding. The consequences on short- and long-term population dynamics and trends as well as the underlying mechanisms are, however, often unknown. Using long-term data from Finland, we demonstrate that black grouse (Tetrao tetrix) have responded to spring warming by advancing both egg-laying and hatching. However, early summer (the time of hatching) has not advanced, and chicks have to face colder post-hatching conditions. Demonstrating that these conditions are critical to post-hatching survival, we show that chicks are increasingly suffering higher mortality because they hatch too early. Consequently, breeding success and population size has severely declined over the past four decades. Finally, we modelled the impact of this particular climate change scenario on population dynamics and show that the mismatch can further explain the observed collapse of cyclic fluctuations. Because the evolutionary response of grouse is lagging behind the novel selective pressures, seasonally asymmetric climate change is likely to constitute an important determinant of future short- and long-term changes in the dynamics of black grouse populations.

Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks.

Avian eggs contain considerable amounts of maternal yolk androgens, which have been shown to beneficially influence the physiology and behaviour of the chick. As androgens may suppress immune functions, they may also entail costs for the chick. This is particularly relevant for colonial species, such as the black-headed gull (Larus ridibundus), in which the aggregation of large numbers of birds during the breeding season enhances the risk of infectious diseases for the hatching chick. To test the effect of maternal yolk androgens on the chick's immune function, we experimentally manipulated, in a field study, yolk androgen levels within the physiological range by in ovo injection of either androgens (testosterone and androstenedione) or sesame oil (control) into freshly laid eggs. We determined cell-mediated immunity (CMI) and humoral immunity of the chicks at the beginning of the nestling period to evaluate early modulatory effects of yolk androgens on immune function. Embryonic exposure to elevated levels of androgens negatively affected both CMI and humoral immunity in nestling gull chicks. Consequently, maternal yolk androgens not only entail benefits of enhanced competitiveness and growth as previously shown, but also costs in terms of immunosuppression. The outcome of embryonic yolk androgen exposure thus likely depends on the post-hatching circumstances for the developing offspring such as parasite exposure and degree of sibling competition.

Genetic and environmental variation in antibody and t-cell mediated responses in the great tit.

Host parasite coevolution assumes pathogen specific genetic variation in host immune defense. Also, if immune function plays a role in the evolution of life history, allocation to immune function should be heritable. We conducted a cross-fostering experiment to test the relative importance of genetic and environmental sources of variation in T-cell mediated inflammatory response and antigen specific antibody responses in the great tits Parus major. Cell mediated response was measured during the nestling period and antibody response against two novel antigens was measured in two-month-old juveniles raised in a laboratory. We found no effect of nest of origin, but a strong effect of rearing environment on cell mediated response. In contrast, we found a large effect of nest of origin on antibody response to both, diphtheria and tetanus antigens suggesting genetic variation. In a model where responses to both antigens were analyzed simultaneously, we found a significant origin-by-antigen interaction, suggesting that genetic variation in antibody responses is specific to particular antigens. Large genetic variation in antibody responses found in this study suggests that host immune defense may evolve and specificity of genetic variation in antibody responses suggests that host defense may be pathogen specific as models of host-parasite coevolution suggest. Our results also suggest that different immune traits are to some degree independent and outcome of the interactions between immune function and the environment may depend on the particular immune trait measured.

Decreased sexual signalling reveals reduced viability in small populations of the drumming wolf spider Hygrolycosa rubrofasciata.

One of the important goals in conservation biology is to determine reliable indicators of population viability. Sexual traits have been suggested to indicate population extinction risk, because they may be related to viability through condition dependence. Moreover, condition-dependent sexual traits may be more sensitive indicators of population viability than early life-history traits, because deleterious fitness effects of inbreeding tend to be expressed mainly at the end of the species' life history. However, empirical evidence of the significance of sexual behaviour for population viability is missing. In this study, we examined two male sexual traits and survival in 39 different-sized and isolated natural populations of the wolf spider, Hygrolycosa rubrofasciata. We also used several traits to estimate female reproductive success in 25 populations of H. rubrofasciata. According to previous studies, H. rubrofasciata males have a costly and condition-dependent acoustic signal, courtship drumming, which is the target of female choice. Males with a high drumming rate have considerably higher viability than males with a low drumming rate, and females that mate with the more actively drumming males gain genetic benefits in terms of increased offspring viability. Our results show that males in small populations had both lower survival and lower drumming rate than males in larger populations. However, we did not find any evidence for a decline in important early life-history traits (offspring number, hatching success or offspring body mass) or female body mass in small populations. Our results have two important messages for conservation biology. First, they show that sexual traits can be used as sensitive indicators of population viability. Second, the indirect benefits of female choice in terms of good genes might partially compensate for the reduction of viability in declining populations. Also, our results support the view that deleterious effects of small population size are expressed at the end of the species' life history.

Adaptive significance of synchronous chorusing in an acoustically signalling wolf spider.

Synchronous sexual signalling is a behavioural phenomenon that has received considerable theoretical interest, but surprisingly few empirical tests have been conducted. Here, we present a set of experiments designed to determine (i) whether the sexual signalling of the drumming wolf spider Hygrolycosa rubrofasciata is synchronous, and (ii) whether the synchrony may have evolved through female preference. Using controlled playback experiments, we found that males actively synchronized their drumming bouts with other males and females significantly preferred closely synchronized drumming clusters compared with loose clusters. In loose clusters, the first drumming signals attracted the most female responses, whereas in close clusters, the last drumming signals were the most heeded. We suggest that this female preference for the last drummer can maintain male synchronous signalling in H. rubrofasciata.

The effect of alternative prey on the dynamics of imperfect Batesian and Müllerian mimicries.

Both Batesian and Müllerian mimicries are considered classical evidence of natural selection where predation pressure has, at times, created a striking similarity between unrelated prey species. Batesian mimicry, in which palatable mimics resemble unpalatable aposematic species, is parasitic and only beneficial to the mimics. By contrast, in classical Müllerian mimicry the cost of predators' avoidance learning is shared between similar unpalatable co-mimics, and therefore mimicry benefits all parties. Recent studies using mathematical modeling have questioned the dynamics of Müllerian mimicry, suggesting that fitness benefits should be calculated in a way similar to Batesian mimicry; that is, according to the relative unpalatability difference between co-mimics. Batesian mimicry is very sensitive to the availability of alternative prey, but the effects of alternative prey for Müllerian dynamics are not known and experiments are rare. We designed two experiments to test the effect of alternative prey on imperfect Batesian and Müllerian mimicry complexes. When alternative prey were scarce, imperfect Batesian mimics were selected out from the population, but abundantly available alternative prey relaxed selection against imperfect mimics. Birds learned to avoid both Müllerian models and mimics irrespective of the availability of alternative prey. However, the rate of avoidance learning of models increased when alternative prey were abundant. This experiment suggests that the availability of alternative prey affects the dynamics of both Müllerian and Batesian mimicry, but in different ways.

Trade-offs between sexual advertisement and immune function in the pied flycatcher (Ficedula hypoleuca).

Good genes models of sexual selection assume that sexual advertisement is costly and thus the level of advertisement honestly reveals heritable viability. Recently it has been suggested that an important cost of sexual advertisement might be impairment of the functioning of the immune system. In this field experiment we investigated the possible trade-offs between immune function and sexual advertisement by manipulating both mating effort and activity of immune defence in male pied flycatchers. Mating effort was increased in a non-arbitrary manner by removing females from mated males during nest building. Widowed males sustained higher haematocrit levels than control males and showed higher expression of forehead patch height, suggesting that manipulation succeeded in increasing mating effort. Males that were experimentally forced to increase mating effort had reduced humoral immune responsiveness compared with control males. In addition, experimental activation of immune defence by vaccination with novel antigens reduced the expression of male ornament dimensions. To conclude, our results indicate that causality behind the trade-off between immune function and sexual advertisement may work in both directions: sexual activity suppresses immune function but immune challenge also reduces sexual advertisement.

Founder population size and number of source populations enhance colonization success in waterstriders.

Understanding the factors that underlie colonization success is crucial both for ecological theory and conservation practices. The most effective way to assess colonization ability is to introduce experimentally different sets of individuals in empty patches of suitable habitat and to monitor the outcome. We translocated mated female waterstriders, Aquarius najas, into 90 streams that were not currently inhabited by the species. We manipulated sizes of propagules (from 2 to 16 mated females) and numbers of origin populations (one or two). Three origin populations were genetically different from each other, but they were less than 150 km from the streams of translocation. The results demonstrate clearly that both the larger propagule size and the high number of source populations have positive effects on the probability of colonizing a new stream. Thus, in addition to the stochastic factors related to the propagule size it may be essential to consider also the diversity of genetic origin for colonization success.

Inbreeding depression and male fitness in black grouse.

The male lifetime lekking performance was studied, and related to inbreeding-outbreeding in a wild population of black grouse (Tetrao tetrix) in central Finland between 1989 and 1995. Inbreeding was measured as the mean heterozygosity and mean d(2) of 15 microsatellite loci. We found a significantly positive relationship between mean d(2) and lifetime copulation success (LCS), while the relationship between heterozygosity and LCS was close to significant. We also found that males that never obtained a lek territory had significantly lower mean heterozygosity than males that were observed on a territory at least during one mating season in their life. Furthermore, among males that were successful in obtaining a lek territory, LCS and mean d(2) were highest for those males that held central territories. We suggest that inbred males have a disadvantage (or outbred males have an advantage) in the competition for territories that may explain the relationships with LCS and inbreeding. Furthermore, the fact that mean d(2) was positively correlated with LCS whereas heterozygosity was not when we restricted the analysis to territorial males, suggests that mean d(2) provides more information about levels of inbreeding-outbreeding than heterozygosity alone, and potentially highlights the effects of heterosis. To our knowledge, this is the first time that measures of inbreeding and lifetime fitness have been linked in a non-isolated population. This is important in establishing that the relationships found in previous studies are not artefacts of low gene flow created by limited dispersal but a general feature of wild vertebrate populations.

Do female leaf beetles Galerucella nymphaeae choose their mates and does it matter?

The role of active female choice in sexual selection is frequently difficult to ascertain, and this is particularly the case for many insect species. Also, it is uncertain whether choosing between males would affect offspring viability. We designed an experiment to investigate the presence of female choice in a Coleoptera species (Galerucella nymphaeae). We also estimated whether mate choice would have any effect on offspring performance. Females were first placed with two males in a test arena to see which of the males copulated with the virgin female, and how quickly. Subsequently the loser male was offered a new virgin female to test for any change in latency time until mating. The two-male tests indicated that males with wider upper prothoraxes were more likely to mate with the female, and the latency time until mating was shorter when the winner male had relatively long wings. When the loser males were placed singly with females the latency time was not correlated with male size, and was the same as when two males were used. These results suggest that male-male competition is the most likely cause of sexual selection on size, and if females have any preferences they are not very strong. The seemingly passive female strategy may be sufficient to ensure that females mate with the most vigorous males, since in the field several males usually compete for access to each female. Finally, the benefits of female choosiness were estimated to be low and non-significant. The eggs of the winner males were no more likely to hatch, offspring survival into adulthood was no greater among descendants of winner males, and the offspring did not differ in adult size.

SEXUAL SELECTION IN A WOLF SPIDER: MALE DRUMMING ACTIVITY, BODY SIZE, AND VIABILITY.

Females are often believed to actively choose highly ornamented males (males with extravagant morphological signals or intense sexual display), and ornaments should be honest signals of male viability. However, this belief is relying only on some pieces of empirical evidence from birds. Our study reports active female choice on sexual display that indicates male viability in spiders. We established trials in which we studied female choice in relation to male courtship drumming activity and body size. Females chose the most actively drumming males as mating partners, but the body size of the males did not seem to be selected. Male drumming activity turned out to be a good predictor of male viability, whereas male viability was independent of male body mass. Our results suggest that by actively choosing mates according to male drumming performance, but independently of male body mass, females are preferring viable males as mates. Because Hygrolycosa rubrofasciata males do not provide obvious direct benefits to their offspring, females may gain some indirect benefits; offspring may have higher chance of survival, or the offspring may inherit the attractiveness of their father.