Scent-rubbing and status signalling by male mammals

Summary There is no consensus about the function of scent-rubbing, a widespread behaviour in which mammals rub their bodies vigorously in substances, many strong-smelling and some artificial, such as rotting meat, intestinal contents and engine oil. Here we suggest that scent-rubbing is involved in status advertisement and that, as in assessment using scent marks, the mechanism used by competitors to assess potential opponents may be scent-matching. In scent-matching a resource holder is assessed (identified) by comparing its odour with odours on or near the defended resource. In scent marking the odour originates from the resource holder (glandular secretion, urine and faeces); in scent-rubbing the odour originates in the environment.A prerequisite of unambiguous scent-matching is that the odour of scent-marks should be uniquely characteristic of one individual. This may be why marking substances are very complex chemically. Scent-rubbing often occurs with scent-marking and, rather than acting independently of scent-marking, the odours acquired may either (i) add to the complexity of the signal, thus reducing signal ambiguity, or (ii) increase the range of the signal by adding a strong smelling component.Subordinates could potentially cheat by rubbing in the same odours as the resource holder. Resource holders could prevent cheating (i) by checking other status cues and by testing competitors whose scent matches, then escalating contests when the competitor's fighting ability (more formally, Resource Holding Power) proves to be lower than that of a resource holder and (ii) by mixing the substances used for scent-rubbing with the unique substances used in scent-marking.     

Testosterone and sexual signalling in male house sparrows (Passer domesticus)

Female preference for mates with elaborated ornaments has often been explained on the basis that exaggerated secondary sexual traits might reflect individual quality and females might gather direct and indirect benefits in mating with such males. Sexual signals must however also entail costs to be reliable indicators of male quality. Androgens have been suggested as a physiological link between sexual signals and individual quality for several reasons, including their immunosuppressive effect. In this study, we tested two hypotheses linked to the hormonal basis of sexual signal expression. First, we investigated whether testosterone is correlated with the size of the black feather bib on the throat of male house sparrows (Passer domesticus) - a trait involved in intra- and inter-sexual selection. Second, we tested whether testosterone affects the seasonal exposure of the trait. Observational work conducted in 1998 showed that the testosterone level was positively correlated with badge size both in spring and in the subsequent fall, after molt. In 1999, we experimentally reduced spring testosterone levels using silastic implants filled with cyproterone acetate, an antiandrogen. Male house sparrows implanted with cyproterone acetate showed reduced exposure of the badge, because the white tips of the black feathers of the badge wore off later than in control males implanted with empty silastic tubes. This result suggests that testosterone can be causally involved in the expression of a secondary sexual trait in house sparrows, at least in terms of its seasonal exposure.     

Life history costs of olfactory status signalling in mice

Large body size confers a competitive advantage in animal contests but does not always determine the outcome. Here we explore the trade-off between short-term achievement of high social status and longer-term life history costs in animals which vary in competitive ability. Using laboratory mice, Mus musculus, as a model system, we show that small competitors can initially maintain dominance over larger males by increasing investment in olfactory status signalling (scent-marking), but only at the cost of reduced growth rate and body size. As a result they become more vulnerable to dominance reversals later in life. Our results also provide the first empirical information about life history costs of olfactory status signals. Received: 15 December 1999 / Revised: 6 June 2000 / Accepted: 24 June 2000     

An experimental study on the causal relationships between (ecto-)parasites, testosterone and sexual signalling

Bird song is considered to have evolved via sexual selection and should as such honestly signal aspects of the quality of its bearer. To ensure honesty, the immunocompetence handicap hypothesis proposed a dual role of testosterone, having positive effects on sexual signalling but suppressive effects on immune function. However, recent studies showed that it is rather an immune activation that suppresses the androgen production. This reversed chain of causation may significantly alter the pathways, which translate the effects of parasites and pathogens into changes in the expression of male sexual traits. We infested male canaries with Ixodes ricinus tick nymphs to investigate the causal relationships between (ecto-)parasites, testosterone and sexual signalling, here singing behaviour. We focused on flexible song traits, which may quickly reflect changes in the infestation status, and tested whether these effects relate to changes in the plasma testosterone levels or health state. The experimental tick infestation altered the males’ song performance by reducing song consistency, a trait that had previously been identified to reflect male quality. The tick infestation lowered the plasma testosterone levels and had a negative effect on the health status in terms of a reduced hematocrit. Our pathway analysis then revealed that it is the parasite-induced reduction of the plasma testosterone levels but not of the health state that caused the changes in song consistency. Thus, our study supports the view that it is the effect of parasites and immune activation on plasma testosterone levels that generates the trade-off between immunocompetence and sexual signalling.     

Body temperature and body size affect flight performance in a damselfly

Flight performance is undoubtedly an important factor for behavioral success in flying insects. Though it is well-known that the flight performance is influenced by body temperature and body size, the relative importance of these factors is not well-understood. We performed laboratory experiments using the male-polymorphic damselfly Mnais costalis with larger territorial males and smaller non-territorial males in a population. We analyzed the effects of body temperature and body size, measured as the thoracic temperature and left hind-wing length, respectively, on two indices of flight performance: maximum lifting force and size-corrected lifting force. The latter is an index of acceleration that is related to aerial agility. The results showed that higher body temperature produced both larger maximum lifting force and larger size-corrected lifting force. In contrast, while larger size produced a larger maximum lifting force, it produced a lower size-corrected lifting force. The results of field measurements showed that territorial males had variable thoracic temperatures depending on the insolation in their territories. In contrast, non-territorial males had less variable and generally higher thoracic temperatures than territorial males as they are mostly found in sunny spots. Until now, the influence of body temperature on behavioral performance has remained unclear although considerable studies have suggested such influence. We showed, here, for the first time, combined effects of body size and body temperature on flight performance. We also showed that body temperature was influenced by the mating strategies of a damselfly. These findings provide new insights into the cost and benefits of territorial behavior in ectothermic animals.     

Cluttered habitats reduce wing asymmetry and increase flight performance in European starlings

Fluctuating asymmetry is a measure of developmental instability and results from both genomic and environmental influences. Levels of asymmetry are (in part) influenced by mechanical constraints, as asymmetry is believed to reduce efficiency. Here we have investigated the influence of habitat structure (“open” and “cluttered” environments) on primary flight feather asymmetry and flight performance in European starlings. Our findings indicate that the increased flight demands of cluttered habitats act to reduce primary asymmetry and increase flight performance. These data are discussed in terms of the influence of asymmetry on flight performance and the mechanisms that give rise to asymmetry. This study also presents a novel method, i.e., examining within-individual changes in asymmetry, by which the detrimental and positive influence of the environment could be studied in subsequent field and laboratory studies without confounding environmental effects with genomic influences. Received: 16 June 1997 / Accepted after revision: 28 December 1997     

Delayed plumage maturation in Lazuli buntings: tests of the female mimicry and status signalling hypotheses

The evolutionary importance of delayed plumage maturation (DPM) in passerines, the condition when more than 1 year is required to achieve adult-like coloration, remains highly contentious. Adaptive hypotheses propose that aggression from after 2nd-year (ASY) males or predation favors DPM in 2nd-year (SY) males, thereby increasing SY male survivorship or reproductive success. However, each hypothesis suggests a distinct selective mechanism explaining “how” this is accomplished. Alternatively, DPM may be a consequence of a nonadaptive molt constraint. We tested the female mimicry and status signalling hypotheses in territorial ASY male lazuli buntings (Passerinaamoena) using three sets of model presentation experiments. The female mimicry hypothesis proposes that dull SY male plumage deceptively mimics female plumage, and predicts that ASY males can not distinguish SY male from female plumage. The status signalling hypothesis proposes that dull SY male plumage honestly signals low competitive threat, and predicts that ASY males respond less aggressively to dull versus bright, ASY-like plumage. Contrary to the female mimicry hypothesis, ASY males distinguished between SY male and female plumage, as they were aggressive to SY male models exclusively and attempted to copulate with female models. Supporting the status signalling hypothesis, ASY males were significantly less aggressive to SY versus ASY male plumage. While DPM may result from a physiological constraint on bright SY male plumage, our results support the idea that dull plumage in an SY male's first breeding season may be maintained by selection to reduce aggression from ASY males, serving as a signal of competitive status. Received: 21 February 1997 / Accepted after revision: 16 June 1997     

Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird

A salient feature of many secondary sexual characteristics in animals is that their expression is controlled by sex-steroid hormones. However, for only a few types of ornaments do we know the precise molecular mechanism by which androgens like testosterone (T) enhance trait production. We studied the red carotenoid-based beak of male zebra finches (Taeniopygia guttata), which serves as a sexually selected trait and is thought to be T dependent. In previous research, we demonstrated that the extent to which male finches produce lipoproteins in the bloodstream, which bind carotenoid pigments acquired from the diet and transport them to peripheral tissues, regulates the accumulation of carotenoids in the body and beak pigmentation. Here we show that T acts to upregulate lipoprotein production and allows male zebra finches to display flashy, sexually attractive coloration. Levels of circulating T in blood positively and significantly predicted lipoprotein profile (as measured by cholesterol levels), blood carotenoid concentration, and beak color. Exogenous T administration elevated cholesterol and carotenoid status as well as beak redness. Last, experimental inhibition of T (using the anti-androgen flutamide) downregulated lipoprotein production and carotenoid circulation and faded the beak. This androgen- and lipoprotein-mediated system represents one of the more detailed physiological mechanisms underlying the development of a sex-steroid-dependent trait in animals.     

Multiple sexual advertisements honestly reflect health status in peacocks (Pavo cristatus)

The evolution of multiple sexual traits remains controversial and poorly understood in evolutionary biology. In many bird species, males exhibit complex courtships involving feather ornaments and behavioral display. Multiple traits may convey information on the genetic and phenotypic quality of males. In particular, fixed characters, such as feather ornaments (produced once a year during the annual molt in many bird species) might convey information about past male condition (at the time of trait development); whereas flexible traits such as behavioral displays should be sensitive to present condition. Here we show that both flexible behavioral displays and fixed feather ornaments of peacocks, used by females to choose a mate, honestly reflect health status. Correlative data showed that peacocks with high display rate (the number of behavioral displays per hour) and a large number of tail eyespots had low levels of circulating heterophils, suggesting better health status. Experimental activation of the immune system, through LPS injection, significantly reduced display rate compared to a control group. However, the sensitivity of a male display rate to the immune challenge was dependent on the number of tail eyespots: males with higher number of tail eyespots were better able to cope with the experimental immune challenge, and maintained their display rate at levels closer to the levels performed before the immune activation. These results are consistent with the idea that multiple signaling might enhance information reliability.     

Timing of arrival from spring migration is associated with flight performance in the migratory barn swallow

Timing of arrival at the breeding grounds by migratory birds affects their mating success and access to superior resources, thus being a major factor associated with fitness. Much empirical work has been devoted to investigate the condition dependence of arrival sequence of migrants and characteristics of individuals that influence arrival time from migration. Surprisingly, there are no studies examining the relationship between flight performance of individual birds and their arrival time. I investigated the relative importance of direct effects of short-term flight performance, age, body condition and the degree of sexual ornamentation (tail length) on timing of spring arrival in the barn swallow (Hirundo rustica), a long-distance trans-equatorial passerine migrant. I evaluated short-term flight performance (a composite variable comprising flight manoeuvrability, velocity and acceleration) in a standardised manner using flight tunnels. Short-term flight performance was a significant and important predictor of spring arrival date. Furthermore, locomotion predicted arrival date of individual birds independently of morphological variables—the degree of sexual ornamentation (the length of the tail) and wing aspect ratio and body condition. I discuss the possible role short-term flight performance may have in determining migratory performance. This is the first time flight performance has been shown to be associated with timing of arrival from migration in a migratory bird.     

Age-dependent effects of carotenoids on sexual ornaments and reproductive performance of a long-lived seabird

Understanding the mechanisms mediating age-dependent reproductive effort in wild animals is a major challenge in evolutionary ecology. The acquisition of molecules able to deter somatic damage could potentially improve reproductive performance, especially in physiologically compromised individuals. Carotenoids are antioxidants and immunoenhancers that animals can only obtain through diet. We tested in male blue-footed boobies whether carotenoid supplementation during incubation improves condition and reproductive performance, particularly of older males. Old birds showed lower levels of peroxidative damage than middle-aged males; however, changes of males' antioxidant capacity and peroxidative damage were not affected by carotenoid supplementation irrespective of age. Experimental old males displayed more colourful feet than control old males after 13 days of first carotenoid supplementation. The effect of carotenoids on male reproductive performance was dependent upon age: young males receiving extra-carotenoids produced chicks with smaller growth rates than control young males, whereas old males receiving extra-carotenoids produced chicks with higher growth rates than control old males. Our results highlight that carotenoids influence the relationship between age and reproductive performance and suggest a positive effect of carotenoids on reproduction of old males.     

Game theory, multi-modal signalling and the evolution of communication

We discuss how the theoretical framework related to selection pressures on multi-component and multi-modal signalling introduced by the article of Wilson et al. in this special issue could usefully be built both theoretically and empirically. Theoretically, we suggest that the game theory approach of Wilson et al. could be generalised using the methodology of adaptive dynamics in order to indicate evolutionary trajectories and paths of evolution. This might indicate the relative likelihood of finding different equilibriums empirically in situations where the game theory explorations of Wilson et al. suggest that multiple equilibriums may exist for a given system. We also suggest how the work of Wilson et al. could be extended theoretically and empirically to further capture the effects of receiver psychology on selective pressures on multi-component and multi-modal signals. We also highlight the assumptions and predictions of the existing theory that would most benefit from and would be most amenable to empirical testing.     

Influence of alternate reproductive tactics and pre- and postcopulatory sexual selection on paternity and offspring performance in a lizard

Sexual selection theory predicts different optima for multiple mating in males and females. We used mating experiments and genetic paternity testing to disentangle pre- and postcopulatory mechanisms of sexual selection and alternate reproductive tactics in the highly promiscuous lizard Eulamprus heatwolei. Both sexes mated multiply: 30–60 % of clutches were sired by two to four fathers, depending on the experiment. Larger males sired more offspring when we allowed male contest competition: 52 % of large males but only 14 % of small males sired at least one offspring. In the absence of male contest competition, females mated promiscuously and there was no large male advantage: 80 % of large males and 90 % of small males sired at least one offspring, and there was no evidence for last-male precedence. Multiple mating did not yield obvious direct or indirect benefits to females. E. heatwolei represents a complex system in which males attempt to improve their fertility success by limiting rivals from access to females and through adopting alternate reproductive tactics. Conversely, females exhibit no obvious precopulatory mate choice but may influence fitness through postcopulatory means by either promoting sperm competition or through cryptic female choice. Our results support the hypothesis that female multiple mating in nonavian reptiles is best explained by the combined effect of mate encounter frequency and high benefits to males but low costs to females.     

Same-sex sexual behavior in insects and arachnids: prevalence, causes, and consequences

Same-sex sexual (SSS) behavior represents an evolutionary puzzle: whilst associated costs seem obvious, positive contributions to fitness remain unclear. Various adaptive explanations have been proposed and thorough reviews exist for vertebrates, but a thorough synthesis of causes for SSS behavior in invertebrates is lacking. Here we provide evidence for such behavior in ~110 species of insects and arachnids. Males are more frequently involved in SSS behavior in the laboratory than in the field, and isolation, high density, and exposure to female pheromones increase its prevalence. SSS behavior is often shorter than the equivalent heterosexual behavior. Most cases can be explained via mistaken identification by the active (courting/mounting) male. Adaptive explanations, such as sperm transfer of the mounting male via the mounted one or gaining experience by young males, are of limited general significance. The passive (being courted/mounted) male is sometimes responsible for this “mistake” by releasing sex pheromones or carrying female pheromones that were attached to his cuticle during prior mating activity. Passive males often resist courting/mating attempts. SSS behavior in arthropods is predominantly based on mistaken identification and is probably maintained because the cost of rejecting a valid opportunity to mate with a female is greater than that of mistakenly mating with a male. Many species exhibiting SSS behavior also mate with related species, another case of mistaken identification. Future research should focus on uncovering the situations/contexts in which mistaken identification is more or less costly for males.     

Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds

Pinnipedia contains some of the most spectacular examples of sexual size dimorphism, examples that are therefore frequently used to illustrate the theory of sexual selection. This paper addresses the question of whether a significant relationship between sexual selection and size dimorphism exists in a comparative context. Thus, harem size and body size data gathered from the literature were analysed with independent contrasts analyses. These investigations showed that sexual size dimorphism is not a consequence of an allometric relationship between male and female size. Instead, there is a clear relationship between harem size and sexual size dimorphism. Further analyses also revealed a significant relationship between harem size and male size whereas no such relationship existed for females. These results support the hypothesis that sexual size dimorphism in pinnipeds is the product of an exclusively male response to sexual selection.     

Sex ratio, sexual dimorphism and mating structure in bethylid wasps

Sexual dimorphism has been linked to parasitoid mating structure by several authors. In turn mating structure has an important influence on predicted sex ratio optima. Here we test the relationship between sexual dimorphism and sex ratio using data from 19 species of bethylid wasps. Using phylogenetically based comparative methods we confirm the findings of a previous cross-species analysis that sex ratio (proportion of males) is strongly and negatively correlated with clutch size. Using cross-species comparisons we show an additional positive correlation of sex ratio and relative male size, as predicted. The relationship however is not significant when using phylogenetically based methods. The cross-species result is largely due to differences between two bethylid sub-families: the Epyrinae have relatively large males and relatively high sex ratios, whereas the Bethylinae have relatively small males and lower sex ratios. Our study illustrates the benefits and drawbacks of using cross-species versus phylogenetically based comparisons. Received: 13 May 1997 / Accepted after revision: 12 January 1998     

Contest behaviour in the speckled wood butterfly (Pararge aegeria): seasonal phenotypic plasticity and the functional significance of flight performance

Although contemporary animal contest theory emphasises the importance of physical asymmetries in resolving disputes, such asymmetries do not obviously settle fights in all groups. Territorial male butterflies, for example, compete via elaborate non-contact aerial interactions in which success is determined by relative persistence. Prior research suggests that the resolution of these contests is not clearly related to physical variables such as body size or energy reserves. However, given that the contests involve elaborate aerial manoeuvres, one long-standing suggestion is that asymmetries in flight performance, and thus flight morphology, may be important. We addressed this hypothesis via a manipulative investigation into the biophysical correlates of contest success in the speckled wood butterfly, Pararge aegeria. This species possesses the ability for significant adaptive phenotypic plasticity in relevant flight morphological parameters. We took advantage of this plasticity to rear 90 individuals of markedly varying flight morphologies, which we then pitted against each other in a semi-controlled experimental fashion. Multiple logistic and lognormal analyses provided little evidence for the relevance of morphological parameters, including relative flight musculature, wing loading and wing aspect ratio (wing length relative to area), to the outcome and/or duration of experimental contests. Instead, we found a positive effect of age upon contest success. Given that ability for high acceleration is strongly linked to variation in these morphological parameters, our findings suggest that flight performance is not a strong determinant of resource-holding potential in this notably territorial butterfly.     

Parasite faunas,testosterone and secondary sexual traits in male red-winged blackbirds

Summary We examined associations among parasite infections, secondary sexual traits and testosterone in male red-winged blackbirds sampled at the start of the breeding season. Parasites quantified included ectoparasitic lice and mites and endoparasitic blood protozoans, nematodes, trematodes and cestodes. Secondary sexual traits that we quantified included body size, epaulet size and color, song repertoire size and song switching rate, and behavioral responses to male and female models. Overall we found few significant associations between parasites and secondary sexual traits, between secondary sexual traits and testosterone, or between parasites and testosterone. In addition, most parasite taxa appeared to infect birds independently, although the low prevalence (<50%) of many of the parasites meant that our sample sizes were too small to detect weak associations. Our most promising results were obtained for ectoparasitic mites, which tended to occur on birds uninfected with other parasites, on birds with longer epaulets, and on birds with higher levels of testosterone. Epaulet length and testosterone are both probable correlates of dominance in this species. Further research will be required to determine whether there is a causal link between the immunosuppressive effects of testosterone and the mite infections, and between testosterone, epaulet length and male mating success. Correspondence to: P. Weatherhead