Chemical ornaments of male lizards <Emphasis Type="Italic">Psammodromus algirus</Emphasis> may reveal their parasite load and health state to females

Evidence for parasite-mediated sexual selection has been found in many species that use visual ornaments to attract females. However, in many animals, variation in female responses to scents of parasitized males suggests that parasitic infections might also affect information conveyed by pheromones (i.e., chemical ornaments). Thus, pheromones might also function in parasite-mediated sexual selection. We show here that female lizards Psammodromus algirus responded differently to femoral gland secretions of males according to the parasite load and health of these males. Scents of healthier males elicited more tongue flicks (a chemosensory behavior) by females, suggesting that these scents were more attractive. Chemical analyses showed that parasite load and the T-cell-mediated immune response were related to the variability in the proportions of some lipids in secretions of males. Further trials testing the chemosensory responses of females to chemical standards indicated that females actually discriminated the chemicals related to males’ health from other chemicals found in secretions. We suggest that these chemical ornaments may provide reliable information on the health and degree of parasitic infection of a male.     

Sexual selection on mature male parr of masu salmon (Oncorhynchus masou): does sneaking behavior favor small body size and less-developed sexual characters?

In many salmonid species, males exhibit morphological dimorphism associated with alternative mating behaviors. ”Precocious males” have a small body size with little or no development of sexual characters and adopt sneaking to gain access to females, while ”migratory males” of large body size and well-developed secondary sexual characters fight. We quantified selection on precocious male parr of masu salmon (Oncorhynchus masou) under simulated natural conditions to examine the contribution of morphology to sneaking success. In contrast to the prediction that sneaking behavior favors small body size, we detected selection favoring relatively large body size for sneaking success. This selection pressure was caused by the dominance hierarchy within parr and may have been facilitated by indifference of dominant migratory males to parr. Unlike the secondary sexual characters exhibited by migratory male salmon, such as the hooked snout and humped back, no morphological characters other than body size contributed to the reproductive success of masu salmon parr. This non-contribution may have been responsible for the lack of development of sexual characters in precocious males. Received: 15 November 1999 / Accepted: 20 May 2000     

Sperm competition risk affects male mate choice copying

Mate choice copying was mostly described as a strategy employed by females to assess the quality of potential mates, but also males can copy other males’ mate choice. An open question in this context is whether and how copying males evaluate sperm competition risk, as mating with a female that has already copulated with another male obviously sets the stage for intense sperm competition (i.e., in species with internal fertilization). Using the livebearing Atlantic molly (Poecilia mexicana) as a model, we asked (a) whether males of that species indeed copy other males’ choices, and if they do so, (b) whether copying males strategically adjust their behavior to sperm competition risk. We used an approach where focal males could first choose to associate with a large or a small stimulus female. Mate choice tests were then repeated after an “observation phase” during which either no model male was present (treatment 1, control) or the previously non-preferred female could be seen associating (treatment 2) or physically interacting (treatment 3) with a model male. We found that, after the observation phase, males spent considerably more time with the previously non-preferred female in treatment (2), i.e., they copied the model male’s choice. This effect was much weaker during treatment (3) where sexual interactions between the model male and the formerly non-preferred female were allowed. Males, therefore, seem to adjust their copying behavior strategically to the perceived risk of sperm competition.     

Do male barn swallows (<Emphasis Type="Italic">Hirundo rustica</Emphasis>) experience a trade-off between the expression of multiple sexual signals?

Some sexual selection models envisage exaggerated male secondary sexual characters to be costly and therefore reliable indicators of the quality of potential mates to choosy females. If male secondary sexual characters have a natural selection cost, they may be linked to each other by reciprocally constraining relationships that would prevent individual males from increasing their level of multiple signaling. Barn swallow (Hirundo rustica) males have at least two costly signals relevant to socio-sexual interactions: tail length and song. Under the hypothesis that a trade-off exists between male signals, we manipulated the maintenance cost of tail ornaments to test whether this reduced the quantity and quality of song, a condition-dependent, phenotypically plastic signal. Contrary to our expectation, tail elongation had no effect on singing activity and song complexity. However, tail-elongated males produced songs with longer terminal parts ('rattles'). Long rattles are associated with highly competitive social contexts and high circulating levels of testosterone, suggesting that tail-elongated males were more frequently involved in either male-male aggressive or inter-sexual interactions. Therefore, this study shows that males are not displaying multiple signals at the maximum possible level, implying that this system is open to unreliable communication. However, long-term trade-offs between signal expression and viability may prevent males from displaying both signals at higher rates.Communicated by: M. Webster     

Looking on the bright side: females prefer coloration indicative of male size and condition in the sexually dichromatic spadefoot toad, <Emphasis Type="Italic">Scaphiopus couchii</Emphasis>

Females across many taxa commonly use multiple or complex traits to choose mates. However, the functional significance of multiple or complex signals remains controversial and largely unknown. Different elements of multiple or complex signals may convey independent pieces of information about different aspects of a prospective mate (the “multiple messages” hypothesis). Alternatively, multiple or complex signals could provide redundant information about the same aspect of a prospective mate (the “redundant” or “back-up” signal hypothesis). We investigated these alternatives using spadefoot toads, Scaphiopus couchii. Spadefoot toads primarily use calls to attract their mates, but males also exhibit sexually dimorphic coloration. We investigated whether male coloration is indicative of male size, condition, or infection status by a socially transmitted monogenean flatworm. We found that male coloration and dorsal patterning predicts male size and condition but not infection status. Moreover, when we presented females with a choice between a bright male model and a dark male model, we found that females preferred the bright model. Because aspects of males’ calls are also associated with male size and condition, we conclude that coloration is a potentially redundant indicator of male phenotype. We suggest that coloration could enhance mate choice in conjunction with male calling behavior by providing females with a long distance cue that could enable them to identify prospective mates in a noisy chorus environment where the discrimination of individual calls is often difficult. Generally, such redundant signals may facilitate mate choice by enhancing the quality and accuracy of information females receive regarding prospective mates.     

Factors predicting male fertilization success in an external fertilizer

In postcopulatory sexual selection both sperm competition and cryptic female choice are considered to be important selective agents, but their relative importance for male fertilization success has received little attention. We tested whether sperm quality, male spawning coloration, male heterozygosity, and genetic overlap with the female explained a male’s fertilization success in controlled in vitro fertilization competition trials between equal numbers of sperm from pairs of male Arctic charr (Salvelinus alpinus), an external fertilizer. Offspring were genotyped to determine each males’ share of paternity. The velocity of a male’s sperm relative to the velocity of the competing male’s sperm was the best predictor of male fertilization success. Yet, sperm velocity was not related to spawning coloration or male heterozygosity. In fact, the most brightly colored male in a pair had the lowest fertilization probability. This could result from cryptic female choice for pale males, but might rather be a result of paler males producing more competitive sperm than more colored males. Furthermore, the more microsatellite alleles a male shared with the female relative to the competing male, the higher fertilization success he had. We argue that this latter may be an effect of assortative cryptic female choice, which might prevent hybridization with sympatric Arctic charr morphs or one form of kin selection.     

A field test of the Hamilton–Zuk hypothesis in the Trinidadian guppy (<Emphasis Type="Italic">Poecilia reticulata</Emphasis>)

The Hamilton–Zuk hypothesis proposes that females prefer male secondary sexual traits because they are honest indicators of parasite resistance. Despite the attention that this hypothesis has received, its role in sexual selection remains equivocal. This study presents the first field test in guppies of two key predictions of the Hamilton–Zuk hypothesis: (1) that within populations, the most highly ornamented males have the fewest parasites and (2) that among populations, males in high parasite populations have the most conspicuous ornaments. Five hundred male guppies from 19 distinct populations in the Northern Range of Trinidad were inspected for Gyrodactylus parasites and photographed. Eight measures of orange spot ornamentation were used to test the predictions: hue, saturation, lightness, relative area, number, and area-weighted hue, saturation, and lightness. Parasite load had no significant effect on any of these measures. There was also no relationship between orange spot ornamentation and parasite abundance among populations. Guppies from high-predation environments had significantly more parasites, and their orange coloration was lighter and less saturated than that in guppies from low-predation environments. Despite previous lab results, this study found no relationship between parasite load and male orange spot ornamentation.     

Offensive and defensive sperm competition roles in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae)

Sperm competition is predicted to generate opposing selection pressures on males. On one hand, selection should favour ‘defensive’ adaptations that protect a male’s ejaculate from displacement, while, on the other hand, selection should favour ‘offensive’ adaptations that overcome paternity assurance mechanisms of rivals. Here, we use the sterile male technique to assess sperm precedence when a male dung beetle Onthophagus taurus mates in both a defensive (first male) and an offensive (second male) role. Significant variation in a male’s sperm precedence (both P ₁ and P ₂) was detected, and an individual’s defensive (P ₁) and offensive (P ₂) abilities were positively correlated. Thus, it appears that sexual selection simultaneously selects for ‘defensive’ and ‘offensive’ adaptations in O. taurus. We discuss a variety of male traits in O. taurus that potentially contribute to a male’s ability to be successful when mating in an ‘offensive’ and a ‘defensive’ role.     

Paternity alone does not predict long-term investment in juveniles by male baboons

Adult male chacma baboons (Papio hamadryas ursinus) form preferential associations, or friendships, with particular lactating females. Males exhibit high levels of affiliative contact with their friends’ infants and defend them from potentially infanticidal attacks (Palombit et al. 1997). Little is known about males’ associations with juveniles once they have passed the period of infanticidal risk. We conducted an observational, experimental, and genetic study of adult male and juvenile chacma baboons in the Moremi Reserve, Botswana. We identified preferential associations between males and juveniles and used behavioral data and a playback experiment to explore whether those associations have potential fitness benefits for juveniles. We determined whether males preferentially invest in care of their own offspring. We also determined how often males invest in care of their former friends’ offspring. The majority of juveniles exhibited preferential associations with one or two males, who had almost always been their mother’s friend during infancy. However, in only a subset of these relationships was the male the actual father, in part because many fathers died or disappeared before their offspring were weaned. Male caretakers intervened on behalf of their juvenile associates in social conflicts more often than they intervened on behalf of unconnected juveniles, and they did not appear to differentiate between genetic offspring and unrelated associates. Playbacks of juveniles’ distress calls elicited a stronger response from their caretakers than from control males. Chacma males may provide care to unrelated offspring of former friends because the costs associated with such care are low compared with the potentially high fitness costs of refusing aid to a juvenile who is a possible offspring.     

Effects of prenatal yolk androgens on armaments and ornaments of the ring-necked pheasant

Mothers may profoundly affect offspring phenotype and performance by adjusting egg components, including steroid hormones. We studied the effects of elevated prenatal testosterone (T) exposure in the ring-necked pheasant on the expression of a suite of male and female traits, including perinatal response to stress, immune response, growth, and secondary sexual traits. Prenatal T levels were increased by injecting the yolk of unincubated eggs with physiological doses of the hormone. Yolk T injection resulted in a reduced length of male tarsal spurs, a trait which positively predicts male success in intra- and intersexual selection and viability, whereas no direct effect on male wattle characteristics or plumage traits of either sex was observed. Female spur length was also negatively affected by T, but to a lesser extent than in males. In addition, the covariation between male secondary sexual traits, which are reliable quality indicators, differed between T and control males, suggesting that the manipulation may have altered the assessment of overall male quality by other males and females. In conclusion, the negative effects of elevated yolk T on spur length, a trait which positively predicts male fitness, coupled with the lack of effects on growth or other traits in both sexes, provided limited evidence for mothers being subjected to a trade-off between positive and negative consequences of yolk T deposition on offspring traits and suggest that directional selection for reduced yolk T levels may occur in the ring-necked pheasant.     

Mating effort and female receptivity: how do male guppies decide when to invest in sex?

Males vary in the degree to which they invest in mating. Several factors can explain this variation, including differences in males’ individual condition and the fact that males allocate their energy depending on the context they face in each mating attempt. Particularly, female quality affects male reproductive success. Here, we studied whether male guppies (Poecilia reticulata) strategically allocated more mating effort, in terms of mating behaviour and male–male competition, when they were matched with a receptive (R) female than a non-receptive one. In accordance with our prediction, we found that males increased their mating behaviour when they were with a receptive female. Even though male guppies can inseminate non-receptive females, we only found high levels of courtship between males that were with a receptive female rather than a non-receptive one. Although there was little affect of female receptivity on male–male competition, we found that males chased and interrupted courtships more with receptive females than with non-receptive females regardless of odour. Finally, we also studied whether the sexual pheromone produced by receptive female guppies is a cue that males use in order to increase their mating effort. We found that males were more attracted to a female when they perceived the sexual pheromone, but only increased their mating and aggressive behaviours when females showed receptive behaviour. This strategic increase in mating effort could result in higher male reproductive success because mating attempts towards receptive females are likely to be less costly and males could have a greater probability of fertilisation.     

Effects of testosterone supplementation on chemical signals of male Iberian wall lizards: consequences for female mate choice

In some lizards, female mate choice is influenced by chemicals secreted by males, e.g., via the femoral glands. Secretions of the femoral glands are under direct androgenic control and vary seasonally with androgen production. However, whether increased testosterone (T) levels affect the concentration and chemical composition of secretions or their attractiveness to females is unknown. We manipulated T levels of male Iberian wall lizards, Podarcis hispanica, with silastic implants. Differential tongue-flick rates indicated that females detected and discriminated between femoral secretions of control and T-implanted males based on chemical cues alone. Females showed greater responses to secretions of T-males, which might suggest that T increased the concentration of chemical signals. Further analyses by gas chromatography–mass spectrometry indicated that T supplementation induced qualitative changes in lipid composition of femoral secretions. T-males had decreased relative proportions of cholesta-5,7-dien-3-ol in secretions, which might be related to the negative effects of T on the immune system and on lipid metabolism. However, experiments of choice of males’ scent showed that females neither preferred nor avoided the scent marks of T-males but preferred males that maintained higher proportions of cholesta-5,7-dien-3-ol in secretions, independently of the experimental manipulation. Thus, because this steroid is negatively affected by T, there might be trade-offs among increasing T levels to increase the production of chemical secretions, maintain metabolism, and attract females.     

Sexual selection in a socially monogamous bird: male color predicts paternity success in the mountain bluebird, <Emphasis Type="Italic">Sialia currucoides</Emphasis>

Ornamental traits are thought to evolve because they give individuals an advantage in securing multiple mates. Thus, the presence of ornamentation among males in many monogamous bird species presents something of a conundrum. Under certain conditions, extra-pair paternity can increase the variance in reproductive success among males, thus increasing the potential for sexual selection to act. We addressed this possibility in the mountain bluebird (Sialia currucoides), a socially monogamous songbird in which males possess brilliant ultraviolet (UV)-blue plumage. Specifically, we asked whether a male’s success at siring offspring within his own nest and within the nests of other males was related to his coloration. In pairwise comparisons, males that sired extra-pair offspring were not more colorful than the males that they cuckolded. However, males that sired at least one extra-pair offspring were, on average, brighter and more UV-blue than males that did not sire extra-pair offspring. Brighter, more UV-blue males sired more offspring both with their own mate and tended to sire more offspring with extra-pair mates and thus sired more offspring overall. Our results support the hypothesis that the brilliant UV-blue ornamental plumage of male mountain bluebirds evolved at least in part because it provides males with an advantage in fertilizing the eggs of multiple females.     

Multiple color signals may reveal multiple messages in male Schreiber’s green lizards, <Emphasis Type="Italic">Lacerta schreiberi</Emphasis>

Multiple traits may either signal different characteristics of a male or be redundant. These multiple signals may convey different messages if they are intended for different receivers (e.g., male or females) that have different interests. We examined the functions of multiple colorful visual traits of male Schreiber’s green lizard (Lacerta schreiberi). Results showed that interindividual variation in the characteristics of coloration of males can be related to variation in morphology, health state, dominance status, and pairing status, but that different relationships were found for each color signal. For example, dominant males had brighter “blue” throat and with higher values of ultraviolet (UV) and bluish coloration and darker and greenish dorsal coloration than subordinate males. Health state was also reflected in coloration; males with a higher immune response had “blue” throats with lower amounts of UV coloration, but had “yellow” chests with higher amounts of UV coloration. Males found guarding females also differed in coloration from males found alone. These data suggest that characteristics of coloration of the different multiple signals may reveal different messages for different receivers, either male or female conspecifics. The development of the different signals, based on different morphological and physiological mechanisms and trade-offs, may allow signal reliability of multiple colorful traits in different social contexts.     

Latency to resume calling after disturbance in the field cricket,<Emphasis Type="Italic"> Teleogryllus oceanicus</Emphasis>, corresponds to population-level differences in parasitism risk

A possible parasitoid-evasion behavioral adaptation is examined in male field crickets, Teleogryllus oceanicus, from three Hawaiian islands where parasitoid prevalence varies naturally among islands. Ormia ochracea, the parasitoid fly that parasitizes T. oceanicus on these islands, uses male calling song to locate its hosts. We used laboratory-reared males from three Hawaiian islands to determine if there are population differences in the time it takes for calling males to resume calling after a standardized disturbance. Males follow the expected pattern; males from the island with the greatest risk of parasitism have the longest latency to resume calling, and males from the island with the least risk of parasitism have the shortest latency to resume calling. Results are discussed in the context of behavioral adaptations to differing parasitism levels, and trade-offs between natural and sexual selection.Communicated by D. Gwynne     

Seasonal variation in the relationship between cellular immune response and badge size in male house sparrows (Passer domesticus)

The immunocompetence handicap hypothesis postulates that secondary sexual traits are honest signals of male quality because steroid hormones (such as corticosteroids and sex steroids), which are supposed to favor the development of secondary sexual traits, may also have immunosuppressive effects. Certain secondary sexual traits are not only used as mate choice signals but also play a role as badges of status. In the house sparrow (Passer domesticus), males have a bib of black feathers which is used both as a signal of social status in male-male interactions and by females when choosing a mate. We investigated the relationships between bib size and cellular immune response in male house sparrows during and outside the reproductive season. Males with large badges were found to have lower levels of immunocompetence, as assessed using a T-cell-mediated immunity assay, during the reproductive season, as predicted by the immunocompetence handicap hypothesis. Conversely, in November, the correlation between badge size and cellular immune response was positive, possibly reflecting the better access to trophic resources of large-badged dominant males in winter flocks. Received: 24 September 1998 / Received in revised form: 2 February 1999 / Accepted: 14 February 1999     

The lemur syndrome unresolved: extreme male reproductive skew in sifakas (<Emphasis Type="Italic">Propithecus verreauxi</Emphasis>), a sexually monomorphic primate with female dominance

The primates of Madagascar (Lemuriformes) are unusual among mammals in that polygynous species lack sexual dimorphism, and females dominate males socially in most species. Moreover, lemur groups are relatively small and characterized by even adult sex ratios despite the fact that one male should be able to exclude other males from the group. One hypothesis to explain this combination of behavioral, morphological, and demographic traits (the “lemur syndrome”) postulates that male–male competition is relaxed and, hence, variance in male reproductive success is low. Reproductive skew theory provides a framework for testing this and several related predictions about lemur social evolution. Specifically, low reproductive skew is also predicted if dominant males or adult females make reproductive concessions to subordinates or if the latter group successfully pursues alternative reproductive tactics. However, suitable data on paternity, demography, and behavior for a conclusive test of these predictions have not been available in the past. In this paper, we show that male reproductive success in ten groups of Verreaux’s sifakas (Propithecus verreauxi) was extremely skewed in favor of the dominant male over 9 years. Our genetic analyses also revealed that more than a third of all groups are effectively harem groups because only one male was unrelated to the resident female(s). In groups with two or more non-natal males, the dominant sired 91% of 33 infants. Together, males pursuing one of several alternative reproductive tactics, such as roaming among several groups or immigrating peacefully, sired only 11% of infants. Thus, female sifakas do not control group composition by offering reproductive opportunities to subordinate males as staying incentives, intrasexual selection is not relaxed, and dominant males prevail in a tug-of-war over subordinate males. Because male reproductive skew in sifakas is even more pronounced than in harem-living anthropoids studied to date, intrasexual selection is clearly not relaxed, and the lemur syndrome is more puzzling than ever.     

Spotted bowerbirds<Emphasis Type="Italic"> Chlamydera maculata</Emphasis> do not prefer rare or costly bower decorations

Females target elaborate secondary sexual traits to acquire either direct benefits, represented or provided by the trait, or indirect benefits usually in the form of genetic components. The link between a males trait and his potential genetic contribution is often unclear. Bowers are extreme examples of secondary sexual traits, built and decorated by males and targeted by females. However, why females should base their mate choice on such structures is unclear. One of the simplest suggestions is that bowers are sites where males exhibit collections of objects that are inherently highly costly, indicating male quality to the choosy female. Such costs can be imposed in two ways, acquisition from the local area, and maintenance in the face of degradation. We studied bowers of spotted bowerbirds Chlamydera maculata at three sites in central Queensland and tested whether components of the bowers that best predict mating success were some of the most costly in the local environment by measuring their abundance, physical dimensions and rate of decay. We also tested whether rare objects per se found on the bowers, were relatively good predictors of mating success. Finally, we experimentally tested whether males preferentially chose rare, and hence costly, objects to use as decorations. We found that objects used on bowers were not unusually costly. Specific objects identified as good predictors of mating success were also some of the more common objects found in the area. They were not the largest objects used on bowers and decayed slowly relative to other objects available for use as decorations. Rare objects in general were not good predictors of mating success and males did not prefer to use rare objects when offered choices. In conclusion, we found no support for the theory that by simply inspecting numbers of decorations and assessing their costs of acquisition and maintenance females can easily obtain information regarding the owners quality. This is due to the fact that decorations used by spotted bowerbirds are not inherently costly.Communicated by J. Graves     

Reproductive trade-offs from mating with a successful male: the case of the tephritid fly Anastrepha obliqua

In lekking species, females may become sperm-limited when mating with sexually successful males, and this may be exacerbated by a poor male diet. Polygynous males may also be limited by the amount of accessory gland products (AGPs) they can transmit to females, which in turn may influence the females’ refractory period and longevity. Here, we tested the effect of male mating history, larval and adult diet on copula duration, mating intervals, female fecundity, fertilisation success, life span and likelihood to remate using sexually successful males of the lekking tephritid fly Anastrepha obliqua. Flies originated from either a native or exotic host fruit and were protein-fed or deprived. Male diet and larval host influenced copula duration, while the time elapsed between matings was affected by the interaction of mating order and male adult diet. Female fecundity was not influenced by female position in mating order or protein inclusion into the male diet. However, mating order and male larval diet influenced female fertilisation success. Importantly, as males mated successively they were less able to induce a refractory period on females, as the last females to mate with a male were more likely to remate and had slightly longer life spans than the first females to mate with males. These results might be attributed to a decrease in male AGPs with increasing male mating frequency. We discuss the role of conditional expression of male mating frequency with respect to A. obliqua’s life history, the trade-off that females face when mating with a successful male, the effect of larval diet on adult sexual performance and the possibility for sexual conflict to occur due to high male mating rates and fitness costs to females.     

Proximal traits and mechanisms for biasing paternity in the red flour beetle Tribolium castaneum (Coleoptera: Tenebrionidae)

A comprehensive understanding of sexual selection requires knowledge of the traits and mechanisms responsible for increasing a male’s paternity share (proportion of progeny sired) relative to that of other males mating with the same female. In this study we manipulated by starvation the expression of traits that might influence male paternity share in Tribolium castaneum. We then conducted experiments to examine how male starvation affects male performance during sequential episodes of sexual selection from mating to progeny production, and investigated female control over specific stages by using live vs dead females. Comparison of starved vs fed males revealed that T. castaneum females have control over spermatophore transfer during mating, as live females rejected inseminations by starved (“low quality”) males. None of the measured male copulatory behaviors (leg-rubbing frequency, asymmetry, and percent of time spent rubbing) affected the probability of successful insemination, but the last two were positively associated with male paternity share. Spermatophore positioning within the female reproductive tract was not affected by male treatment (starved/fed), by female treatment (live/dead), or by male copulatory behaviors. Starvation, however, had a dramatic effect on male reproductive physiology, decreasing both accessory gland size and total number of sperms transferred (but not sperm viability in seminal vesicles). In addition, females who mated to starved males stored fewer sperms in their spermathecae, which, together with decreased ejaculate size, may explain the reduced paternity share of starved males compared to fed males. This study elucidates some cryptic mechanisms influencing male reproductive success and aids our understanding of trait evolution through sexual selection.