Honest Indicators Of Male Quality Research Articles

Imperfect synchrony in animal displays: why does it occur and what is the true role of leadership?

Synchrony can be defined as the precise coordination between independent individuals, and this behaviour is more enigmatic when it is imperfect. The traditional theoretical explanation for imperfect synchronous courtship is that it arises as a by-product of the competition between males to broadcast leading signals to attract female attention. This competition is considered an evolutionary stable strategy maintained through sexual selection. However, previous studies have revealed that leading signals are not honest indicators of male quality. We studied imperfect courtship synchrony in fiddler crabs to mainly test whether (i) signal leadership and rate are defined by male quality and (ii) signal leadership generates synchrony. Fiddler crab males wave their enlarged claws during courtship, and females prefer leading males-displaying ahead of their neighbour(s). We filmed groups of waving males in the field to detect how often individuals were leaders and if they engaged in synchrony. Overall, we found that courtship effort is not directly related to male size, a general proxy for quality. Contrary to the long-standing assumption, we also revealed that leadership is not directly related to group synchrony, but faster wave rate correlates with both leadership and synchrony. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

Female preference for dominant males in the Mexican mojarra cichlid fish, Cichlasoma istlanum.

It is widely assumed that female preference and male competition operate simultaneously during sexual selection. Dominance is likely an honest indicator of male quality, and females can identify and choose the dominant male to reproduce with individuals with greater competitive abilities, thus improving the quality and competitiveness of their offspring. In this context, few studies have investigated female preference in relation to male fighting ability. The Mexican mojarra, Cichlasoma istlanum, is a cichlid species native to the Balsas River basin. It is territorial during reproduction and provides parental care. Males commonly engage in territorial defence, whereas females care directly for offspring. This study examined whether females prefer dominant males that exhibit more aggressive behaviour. The authors conducted experiments using groups of two males and one female to test competitive ability in males and female preference. They also quantified the time during which the female associated with the dominant male and the subordinate male after observing the outcome of a fight between the two males. They found that Mexican mojarra females preferred dominant males and that the time females spent associating with males was positively related with their aggressive behaviours during competition. These results indicate that dominant males were more attractive than subordinate males to female Mexican mojarra. The relationship between female preference and male dominance in the Mexican mojarra demonstrates the importance of male competitive ability for future parental care in reproduction.

Sexual ornaments reveal the strength of melanization immune response and longevity of male paper wasps

It has been recently suggested that female mate choice, based on sexually selected ornaments, is an important component of social wasps’ reproductive biology. The correlates of male ornaments that could be of a female’s interest, however, remain to be investigated. Males of the Neotropical paper wasp Polistes simillimus have sexually dimorphic melanin-based black spots on their faces. In this species, male spots work like sexual ornaments, as it has been experimentally demonstrated that females prefer sexual partners with a higher proportion of black pigment on their faces. We have shown that, under laboratory conditions, male sexual ornamentation positively predicts the strength of the melanization immune response and longevity. Therefore, in P. simillimus, melanin-based facial patterns (ornaments) seem to be honest indicators of male quality.

Courtship behaviour and display-site sharing appears conditional on body size in a lekking bat

Leks are aggregations of sexually displaying males visited by receptive females and characterized by intense male–male competition to attract mates. Success in lekking species is often contingent upon male display output and/or lek attendance, with energetically costly displays functioning as an honest indicator of male quality. Furthermore, display spaces are vigorously defended by territorial males, and territory characteristics are often linked to male phenotype. Here we describe the courtship and territorial behaviour of lekking lesser short-tailed bats, Mystacina tuberculata, and both behaviours appear to be conditional on body size. During the breeding season, lekking males occupy and defend small tree hollows and sing for long periods of the night to attract females. Although some males sing alone, others form ‘timeshare’ singing roosts, where multiple males visit sequentially to sing each night. In our study, solitary males were significantly smaller than timeshare males and individually had both higher song outputs and higher roost occupancy rates, although timeshare roosts had higher overall occupancy rates. There appeared to be no fitness difference between the two male groups, and while one timeshare roost contained relatively closely related individuals (which roost settlement simulations indicate was not a chance event), four did not. We discuss factors that may promote timeshare formation, including competition for access to desired roosts and potential by-product mutualisms. Courtship and sexual selection in bats is largely undescribed, and thus our study provides a useful description of behaviour in a little-studied taxon.

Listening to male song induces female field crickets to differentially allocate reproductive resources

Differential investment in offspring by mothers is predicted when there is substantial variation in sire quality. Whether females invest more resources in the offspring of high-quality mates (differential allocation, DA) or in the offspring of low-quality mates (reproductive compensation, RC) is not consistent in the literature and both effects can be predicted by theoretical models. In the field cricket, Grylluspennsylvanicus Burmeister, 1838 (Orthoptera: Gryllidae: Gryllinae), females are attracted more to calling songs of high-quality males than to those of low-quality males. We tested whether females invest reproductive resources differentially based on perceived mate quality. We manipulated female perception of male quality by allowing virgin females to approach a speaker broadcasting either high- or low-quality calling song (high or low calling effort respectively), and then mated them with a randomly chosen male that had been rendered incapable of calling. In the week following mating, females exposed to high-quality calling song gained less weight, laid more embryos, and laid larger embryos than females exposed to low-quality calling song, although only the first of these effects was statistically significant. These results support the DA hypothesis and suggest that females invest their reproductive output based on a trait (calling effort) that is an honest indicator of male quality.

Urban mountain chickadees (Poecile gambeli) begin vocalizing earlier, and have greater dawn chorus output than rural males

Vocal output during the dawn chorus is often an honest indicator of male quality, where males with greater access to food and in better condition produce more vocalizations. We compare the vocal output among male mountain chickadees living along an urbanization gradient to assess how urbanization affects male signalling. Chickadees forage in the canopy, and because urban habitats are associated with lower canopy volume, we predicted that urban habitats may offer lower food and thus lead to reduced song output. Contrary to our predictions, males in more urbanized habitats had greater vocal output. We suggest that despite decreased canopy cover, urban birds may have greater access to food in both the breeding and pre-breeding seasons due to differences in both supplementary resources and vegetation composition of urban vs rural landscapes in our area. Living in urban habitats may allow males to enter the breeding season in better condition.

Does leadership indicate male quality in Neoconocephalus katydids?

Females of many species show strong directional preferences for costly male signals, which serve as indicators of male quality. Leader preference, a directional preference for males producing their signals ahead of their neighbors’, is unusual in that there are no inherent costs to producing the attractive signal. Nonetheless, interacting males compete to produce leading signals, with the winner gaining a large fitness advantage. Here, we test whether competition to produce leading calls is sufficient to make leadership an honest indicator of male quality in the absence of costs in Neoconocephalus katydids. We include one species with leader preference and two without to determine whether any correlations between signal and quality arose before or after the evolution of leader preference. We found no correlations between leadership and male quality in any species tested, suggesting that the production of leading calls does not serve as an honest indicator of quality. This is likely the ancestral state for this system. The ability to produce leading calls in N. ensiger, the species with leader preference, was not correlated with costly call traits. However, the ability to produce leading calls was highly repeatable, allowing for the possibility that it encodes meaningful information about males. The inter-individual variation in the ability to produce leading calls is likely caused by neural properties within the central pattern generator; this variation is likely due to both genetic and environmental factors. Though we found no evidence that females gain a fitness benefit by mating with leading males, we cannot exclude the possibility without tests of female fitness. Females often show strong preferences for costly male signals that advertise male quality. The preference for males producing signals ahead of their neighbors’ is unusual in that there are not necessarily any energetic costs associated with producing the preferred signals. However, males do compete to produce leading signals, allowing for the possibility that only high quality males can “win” these interactions as some costs become associated with winning. We tested whether the ability to produce leading calls advertises male quality in Neoconocephalus katydids, even in the absence of energetic costs. We found no correlation between the ability to produce leading calls and male quality in any species tested. Though further tests are necessary, this suggests that the ability to produce leading calls does not advertise male quality, even when males are competing for the leading role.

The effect of sire dominance and aggression on fitness measures in a field cricket (Gryllus assimilis)

Theory stipulates that females should prefer to mate with higher-quality mates to maximize their fitness. As such, traits that females prefer should be honest indicators of male quality. Dominant males are often higher quality, and mating with dominant males may confer indirect fitness benefits to females. Male Jamaican field crickets, Gryllus assimilis, fight more aggressively in front of a female audience than when there is no audience present. Males may increase their aggression because females prefer to mate with males who they have seen win a fight. To test this hypothesis we first allowed females to observe (treatment) or not observe (control) fights and then mated females to either fight winners or losers. We then assessed the following fitness measures: number of eggs oviposited, egg viability, offspring viability and offspring size at adulthood. Neither male fight victory status nor female observer/nonobserver status influenced any of the aforementioned female fitness measures; however, the aggressiveness level of the fight did. Females that mated with males that had participated in more aggressive fights produced offspring that were larger at adulthood. Given that females find larger males more attractive, and larger females oviposit more eggs, these larger offspring may experience greater reproductive success and as a result provide females with indirect fitness benefits.

Diet and birdsong: short‐term nutritional enrichment improves songs of adult Bengalese finch males

Song is a notable sexual signal of birds, and serves as an honest indicator of male quality. Condition dependence of birdsong has been well examined from the viewpoint of the developmental stress hypothesis, which posits that complex songs assure fitness because learned acoustic features of songs are especially susceptible to early‐life stress that young birds experience in song learning periods. The effect of early stress on song phenotypes should be crucial, especially in age‐limited song learners which sing stereotyped songs throughout life. However, little attention has been paid to non‐learned song features that can change plastically even in adulthood of age‐limited song‐learners. Although it has been shown that food availability affects song rate in wild songbirds, there is limited evidence of the link between favorable nutritional conditions and song phenotypes other than song rate. Under the prediction that singing behavior reflects an individual's recent life history, we kept adult Bengalese finch males under high‐nutrition or normal diet for a short term, and examined changes in body mass and songs. We found that birds on a high‐nutrition diet showed higher song output (e.g. song rate and length) compared with those of the control group, while changes in body mass were moderate. In addition, note repertoire became more consistent and temporal structures got faster in both nutrition and control groups, which indicates that songs were subject to other factors than nutrition. Considering that female estrildid finches, including Bengalese and zebra finches, show a preference toward complex songs as well as longer songs and higher song rate, it is plausible that different aspects of singing behavior signal different male qualities, and provide multifaceted clues to females that choose mates.

The effect of male dominance on female choice in a field cricket (Gryllus assimilis)

Theory suggests that behaviours previously thought only to influence intrasexual selection, such as aggression between males, can also be co-opted to serve in intersexual selection as honest indicators of male quality. Our previous research revealed an audience effect: male Jamaican field crickets, Gryllus assimilis, fight more aggressively in front of a female audience. One way for this to evolve is if females are more attracted to more aggressive males or fight winners. Given the potential interplay between intra- and intersexual selection, we investigated how observing a fight influences subsequent female mate choice and mating behaviour. We utilized two female treatments: Observers watched the two males fight, whereas Non-observers watched two noninteracting males. We then immediately tested Observer and Non-observer females for their mating preferences towards male fight participants using dichotomous and no-choice tests. Our approach enabled us to assess whether females preferred either dominant (winner) or subordinate (loser) males and whether females gathered information about males while watching them fight that informed their mating preferences. While females did not prefer fight winners over losers in dichotomous choice tests, in the no-choice tests, females were more likely to mount winners and mount males that they had preferred in the dichotomous choice tests. Intra- and intersexual competition appears to be mutually reinforcing in this species, but eavesdropping is unlikely to explain the evolution of audience effects.

Curse of the black spot: spotting negatively correlates with fitness in black grouseLyrurus tetrix

There is growing evidence that achromatic plumage can act as honest indicators of male quality. In some species with areas of white plumage, black melanin spots can be found on parts of the feathers. The functional significance of these spots and the relationship with male quality is yet poorly understood. We investigated the relationship between black melanin spots in an otherwise totally white ornament, the undertail covert, in relation to age, fitness and covariance with past and present expression of sexual traits, in the lekking black grouse Lyrurus tetrix. We found that spots at tips of feathers (tip spots) were negatively related to survival and reproductive success, and covaried negatively with current fighting rate. They also covaried positively with past fighting rate, suggesting high investment in fighting leads to carryover effects on male condition. In contrast, spots found further down the feather (vane spots) were unrelated to fitness and morphological and behavioural trait expression. Our results show that melanin spots can indicate some relationship with male quality and that the location of the spots has some importance in this relationship. However, the exact drivers of melanin spot expression and how these link to male quality, are currently unknown.

Different ornaments signal male health and MHC variation in two populations of a warbler.

Male traits that signal health and vigour are used by females to choose better quality mates, but in some cases the male trait selected by females differs among populations. Multiple male traits can be maintained through female mate choice if both traits are equally honest indicators of male quality, but tests of this prediction are rare. By choosing males based on such traits, females could gain direct benefits from males (assistance with parental care), but when females choose extra-pair mates based on these traits, females gain only male sperm, and potentially indirect genetic benefits for their offspring. In common yellowthroats (Geothylpis trichas), female choice of extra-pair mates targets two different plumage ornaments: the black mask in a Wisconsin population and the yellow bib in a New York population. Previously, we found that the black mask in Wisconsin is related to greater major histocompatibility complex (MHC) class II variation, which in turn signals better survival and disease resistance. In this study, we examined the signalling function of the yellow bib in New York to test whether it signals the same aspects of male quality as the black mask in Wisconsin. As predicted, we found that the yellow bib in New York is most closely associated with MHC variation, which also signals survival and resistance to blood parasites. Thus, the ornament preferred by females differs between the two populations, but the different ornaments signal similar aspects of male health and genetic quality, specifically information regarding MHC variation and potential indirect genetic benefits to females.

Testosterone, body size, and sexual signals predict parasite load in Yarrow’s Spiny Lizards (Sceloporusjarrovii)

Parasite load significantly impacts host health and fitness and may vary substantially among individuals within a population. The immunocompetence handicap hypothesis posits that sexual signals are honest indicators of male quality because they are maintained by testosterone, an immunosuppressant that yields higher parasite loads. Additionally, testosterone may influence parasite load by increasing activity levels. We examined these two hypotheses in a wild population of Yarrow’s Spiny Lizards (Sceloporus jarrovii Cope, 1875) in Arizona. We (i) compared fecal testosterone levels to ectoparasite and haemoparasite loads, (ii) tested if sexual signals (total coloured area, aggression, and head size), locomotor activity, and body size correlated with testosterone levels, and (iii) compared sexual signals, locomotor activity, and body size to parasite load. Ectoparasite loads increased with total coloured area and tended to increase with testosterone, but this latter relationship was only nearly significant. Parasite loads increased with body size. Thus, we found some support for the immunocompetence handicap hypothesis and none for the activity hypothesis. Our results are consistent with an alternative hypothesis that larger individuals have more parasites because they have more surface area and (or) have had longer to accumulate parasites. Future studies should examine the relative contributions of testosterone and glucocorticoids in driving variation in parasite loads.

Buzzwords in Females’ Ears? The Use of Buzz Songs in the Communication of Nightingales (Luscinia megarhynchos)

Differences in individual male birds’ singing may serve as honest indicators of male quality in male-male competition and female mate choice. This has been shown e.g. for overall song output and repertoire size in many bird species. More recently, differences in structural song characteristics such as the performance of physically challenging song components were analysed in this regard. Here we show that buzz elements in the song of nightingales (Luscinia megarhynchos) hold the potential to serve as indicators of male quality and may therefore serve a communicative function. Buzzes were produced with considerable differences between males. The body weight of the males was correlated with one measure of these buzzes, namely the repetition rate of the buzz subunits, and individuals with larger repertoires sang buzzes at higher subunit-rates. A model of buzz performance constraints suggested that buzzes were sung with different proficiencies. In playback experiments, female nightingales showed more active behaviour when hearing buzz songs. The results support the idea that performance differences in the acoustic fine structure of song components are used in the communication of a large repertoire species such as the nightingale.

Female goats use courtship display as an honest indicator of male quality

Due to the differential cost of reproduction in promiscuous species, like domesticated goat(s) (Capra hircus), it is expected that females should mate with higher quality males, while males should mate with a greater number of females. Females may use conspicuous secondary sexual characteristics of males such as courtship display to distinguish among high and low quality males. Testosterone (T) controls a large suite of secondary sexual characteristics and variation in T concentrations may account of differences in courtship rates. Two studies were conducted to examine the relationship between T concentrations and courtship rate and its role in mammalian female mate choice. Experiment 1 utilized bucks (intact males) and Experiment 2 utilized T-replaced wethers (castrated pre-pubertally). During the first year of Experiment 2, T-replaced wethers received either vehicle control (CON), 25mg or 100mg testosterone propionate (TP). During the second year of Experiment 2, T-replaced wethers were treated with either 5mg, 15mg or 25mg TP. For all experiments, mean courtship rates and circulating T concentrations were measured, as well as female preference for males displaying different courtship frequencies. T concentrations and courtship rate were positively correlated for bucks and estrous females preferred high courting bucks. Males receiving 25mg and 100mg TP courted females at a similar rate, but both were significantly higher than courtship rates of the CON wethers. Courtship rates of the 25mg, 15mg and 5mg TP-treated males were all significantly different. Females did not show a preference between the 100mg or 25mg TP-treated wethers, however both were preferred in comparison to the CON wethers. Females did not show preference between the 25mg or 15mg TP-treated wethers, however both were preferred in comparison to the 5mg TP-treated wethers. Taken together, these studies suggest that courtship rate is T-dependent. Further, females can use courtship rate to distinguish among males.

Indicators of development as sexually selected traits: the developmental stress hypothesis in context

The developmental stress hypothesis proposes that the honesty of bird song as a signal may be maintained by costs incurred during development. That is, song complexity or other features of song may be honest indicators of male quality because they reflect an individual's developmental history. Over the last decade much evidence in support of this hypothesis has accrued. Experimentally imposing stressors on songbirds early in development results in impaired development of song and the brain regions controlling song. We review the evidence in support of the developmental stress hypothesis and indicate where information is still lacking. Further, we propose that the developmental stress hypothesis may be specific example of a general process whereby indicators of developmental stability become sexually selected traits. In this light, birdsong and fluctuating asymmetry may have evolved through similar evolutionary processes. Finally, we highlight that a wide range of physiological systems may be simultaneously affected by stress early in life, thus resulting in correlations between sexual ornamentation, such as song and other cognitive and physiological traits. Such traits may indicate different aspects of development. First, traits may signal how well an individual coped with stressors, and could predict indirect genetic benefits to a female. Second, traits may signal the quality of the developmental environment, and could predict direct benefits to a female via developmentally correlated traits. Copyright 2011, Oxford University Press.

Sexual Selection of Male Song in Free-Living Sagebrush Crickets, Cyphoderris Strepitans

Measures of lifetime mating success in the sagebrush cricket, Cyphoderris strepitans, have revealed that most males succeed in obtaining only 1 mating, while many males fail to attract a female at all and a small minority mate 2 to 4 times. Relative to their abundance in the population, virgin males have a greater likelihood of obtaining a mating than non-virgin males have of securing additional matings, a phenomenon known as the virgin male mating advantage. Previous studies of sagebrush crickets have focused primarily on determining the proximate mechanisms responsible for the virgin male mating advantage, but little work has been done to identify the factors that influence male attractiveness in the first place. Because song plays a central role in mate attraction, it’s likely that variability in song parameters among males could account for the observed differences in mating success. Song is an energetically costly signal to produce and could serve as an honest indicator of male quality. Consequently, males that are able to invest greater amounts of energy into singing should be more attractive to females. In a previous field season, we recorded and analyzed the songs of virgin and non-virgin males and indeed found some evidence that females prefer males which invest greater energy into calling. In the present study, we synthesized artificial sagebrush cricket songs and directly measured female song preference with an arena playback experiment. Females were shown to consistently prefer song characteristics that would require greater energy expenditure by males. Males that sing with long pulse duration, long train duration, and at an intermediate dominant frequency were found to be highly attractive to females.

Functionally opposing effects of testosterone on two different types of parasite: implications for the immunocompetence handicap hypothesis

Summary 1. The immunocompetence handicap hypothesis (ICHH) proposes that androgen‐dependent sexual traits are honest indicators of male quality because androgens are thought to suppress the immune system’s ability to combat parasitic infection. Yet, recent work suggests that the relationship between androgens and parasitism is more complex, as androgens may have different effects on the various types of parasites. 2. We explored this issue in free‐living mountain spiny lizards, Sceloporus jarrovi, by measuring the prevalence of four endoparasite species and one ectoparasite species in castrated, sham‐operated and testosterone (T)‐implanted males. 3. We found that effects of T manipulation accounted for the greatest amount of variability in the abundance of Trombiculid mites and two gastrointestinal nematodes (Physaloptera retusa and Spauligodon giganticus). Plasma T levels were positively associated with mite loads, negatively associated with P. retusa loads and not associated with S. giganticus load. We also found that T treatment had little effect on the abundances of two species of blood‐borne endoparasites (Plasmodium chiricahuae and an unidentified haemogregarine). Instead, the prevalence of these two parasites was mostly influenced by other physiological or seasonal factors, such as corticosterone levels, body condition, fat stores or time between capture events. 4. Our data illustrate that T can have functionally distinct and opposing effects on different parasite species. This finding supports the hypothesis that T does not depress the immune system in a way that causes an across‐the‐board increase in parasitism. 5. We speculate that T modifies select behavioural and physiological factors that govern parasite accumulation. Evolutionarily, our data also imply that the net ‘cost of T’ with respect to elevated ectoparasitism may be at least partially offset by concomitant reductions in helminth load.

Achieving luster: prenuptial molt pattern predicts iridescent structural coloration in Blue-black Grassquits

Colors in feathers are produced by pigment deposition or by nanostructures within barbs or barbules. In the absence of pigments or nanostructures, light is scattered incoherently, producing white coloration. Honest advertisement models predict that ornamental colors evolve if they reliably signal individual properties such as viability, health, or nutritional state. In this study, we tested if (1) iridescent structural and (2) unpigmented plumage coloration signal male quality in the Blue-black Grassquit (Volatinia jacarina). During three reproductive seasons, we captured males and measured morphological variables and nuptial plumage coverage, and collected feathers for spectrometry. We found that saturation of the iridescent coloration was positively related to relative molting speed, indicating that males investing more in prenuptial molt also produced more saturated, UV-shifted plumage. Body condition was not related to brightness or saturation of the iridescent plumage, and no male morphological attributes were associated with the white underwing patch coloration or size. Our results suggest that patterns of molt, and possibly feather growth, may affect the organization of optical nanostructures responsible for iridescent coloration, and that the ontogeny of iridescent plumage ornaments must be taken into account in hypotheses concerning honest advertisement of such signals. Thus, coloration in this species may reliably reflect energy allocation to molting, constituting an honest indicator of male quality, life history decisions, or endocrine state. To our knowledge, this is the first report of natural variation in molting pattern being associated with sexually-selected structural color plumage.

Bluegill Coloration as a Sexual Ornament: Evidence From Ontogeny, Sexual Dichromatism, and Condition Dependence

AbstractIn aquatic environments, visual communication is expected in animals that inhabit clear, shallow waters. Here, we investigate variation in the colorful traits of bluegills, Lepomis macrochirus, to elucidate their possible function. Bluegills use alternative mating tactics whereby males develop into one of two irreversible phenotypes termed parental and cuckolder. Parentals build and defend nests and care for offspring whereas cuckolders obtain matings by sneaking copulations. We hypothesized that bluegill coloration might function as a sexual ornament in parental males and that ornamental coloration might serve as an honest indicator of male quality. We predicted that coloration should be more pronounced in parental males than in females and immature males and should be more pronounced during the breeding season. We also predicted that males in better condition should be more intensely colored than fish in poor condition. To test our predictions, we sampled 510 bluegills during the breeding and post‐breeding seasons at nine lakes in southern Ontario, Canada, in 2007. We used reflectance spectrometry to quantify the coloration of five body regions, aged and sexed each fish, and calculated Fulton’s condition factor from morphological measurements. A separate experiment showed that color did not fade several minutes post capture, suggesting that coloration could be measured reliably and consistently. We found that color was influenced by maturity, sex, and season, in the predicted direction, for three body regions (breast, cheek, and opercular flap). We also found that color varied with the condition of males such that males in better condition were darker for the sexually dichromatic ventral and facial regions. Our findings therefore suggest that some colorful traits in bluegills may serve as condition‐dependent sexual signals during the breeding season. Our research contributes to a growing appreciation of the importance of visual signaling in aquatic environments.