Multiple Male Traits Research Articles

Multiple phenotypic traits predict male mating success in a critically endangered frog

Complex sexual signals spanning multiple sensory modalities may be common in nature, yet few studies have explored how combinations of phenotypic traits influence male attractiveness and mating success. Here, we investigate whether combinations of multiple male phenotypic traits (both within and across sensory modalities) predict male mating and fertilization success in the critically endangered southern corroboree frog, Pseudophryne corroboree. We conducted breeding trials in a standardized captive environment where females were given the opportunity to choose between multiple males over the duration of the breeding season. For each male, we measured multiple call traits, aspects of coloration, body size, and age. We found that complex interactions between multiple traits best predicted male mating and fertilization success. In general, males with lower call frequency, lower call rate, and shorter call duration had the highest mating and fertilization success. Fertilization success was additionally linked to male body size and age. These findings suggest that female P. corroboree select mates based on a suite of acoustic traits, adding to a growing body of evidence that females use multiple traits to assess male quality. Our results also suggest that females may combine information from multiple signals non-additively. Moreover, our results imply that females gain direct fertility benefits from their mate choice decisions. We argue that understanding female mate choice based on various signals across multiple sensory modalities has important implications for the integration of mate choice into conservation breeding programs and needs to be considered when developing behavior-based captive breeding strategies.Significance statementSexual signals are often highly complex, yet we know little about how multiple signal components both within and across various sensory modalities predict male mating success. We investigated whether combinations of multiple phenotypic traits (within and across sensory modalities) predicted male breeding success in threatened corroboree frogs. We conducted captive breeding trials in a homogeneous environment, where females could choose between multiple males over the duration of a single breeding season. We found that interactions between multiple male traits predicted mating and fertilization success. Males with lower call frequency, call rate, and duration had higher mating success. Fertilization success was also linked to acoustic signals, body size, and age. Understanding mate choice for multiple traits further elucidates the complexity of female mate choice. This study is one of the first to consider the conservation implications of multimodal signaling in mate choice.

Increased pheromone signaling by small male sea lamprey has distinct effects on female mate search and courtship

Male body size affects access to mates in many animals. Attributes of sexual signals often correlate with body size due to physiological constraints on signal production. Larger males generally produce larger signals, but costs of being large or compensation by small males can result in smaller males producing signals of equal or greater magnitude. Female choice following multiple male traits with different relationships to size might further complicate the effect of male body size on access to mates. We report the relationship between male body size and pheromone signaling, and the effects on female mate search and courtship in the sea lamprey (Petromyzon marinus). We predicted that pheromone production in the liver and the liver mass to body mass ratio would remain constant across sizes, resulting in similar mass-adjusted pheromone release rates across sizes but a positive relationship between absolute pheromone release and body mass. Our results confirmed positive relationships between body mass and liver mass, and liver mass and the magnitude of the pheromone signal. Surprisingly, decreasing body mass was correlated with higher pheromone concentrations in the liver, liver mass to body mass ratios, and mass-adjusted pheromone release rates. In a natural stream, females more often entered nests treated with small versus large male odors. However, close-proximity courtship behaviors were similar in nests treated with small or large male odors. We conclude that small males exhibit increased release of the main pheromone component, but female discrimination of male pheromones follows several axes of variation with different relationships to size. Large males often produce signals that are more attractive to females. We determined the relationship between male body size and pheromone signaling in the sea lamprey (Petromyzon marinus). We predicted that larger males, who have a larger pheromone-producing organ, would have a larger pheromone signal and that females, who prefer larger pheromone signals, would prefer the odor of large males. Surprisingly, we found that mass-adjusted pheromone release rates increase with decreasing male body mass due to higher rates of pheromone synthesis and a slightly larger liver proportional to total body mass. In a natural stream, small male odors attracted more females but elicited similar courtship behaviors compared to large male odors.

Females can solve the problem of low signal reliability by assessing multiple male traits.

Male signals that provide information to females about mating benefits are often of low reliability. It is thus not clear why females often express strong signal preferences. We tested the hypothesis that females can distinguish between males with preferred signals that provide lower and higher quality direct benefits. In the field cricket, Gryllus lineaticeps, females usually prefer higher male chirp rates, but chirp rate is positively correlated with the fecundity benefits females will receive from males only for males that have experienced low quality diets. We paired females with muted males that were maintained on low or high nutrition diets, during the interactions we broadcast a replacement high chirp rate, and we observed whether females mated with the assigned male. Females were more likely to mate when paired with low nutrition males. These results suggest that females have evolved assessment mechanisms that allow them distinguish between males with preferred signals that provide high quality benefits (low nutrition males with high chirp rates) and males with preferred signals that provide low quality benefits (high nutrition males with high chirp rates).

Genetic variation in male attractiveness: It is time to see the forest for the trees.

Female choice based on multiple male traits, rather than on any single one, has been reported in many species and may well be a rule rather than an exception. However, the implications this has for selection acting on choosiness itself remain underappreciated. We argue that this constitutes one of the important impediments to our understanding of the evolution of mate choice. We discuss this issue primarily in the context of the Fisherian model of sexual selection. We review theory and empirical data, showing how the crucial parameter of the model-genetic variation in male attractiveness-can be estimated when attractiveness is a function of multiple traits. Based on the reviewed theory, we show how relying on individual male traits, instead of overall attractiveness, can produce biased estimates of Fisherian benefits of female choice. This bias can be substantial, especially when many traits contribute to male attractiveness. We discuss a number of methodological issues that, we hope, will stimulate future studies and help resolving the long-standing mystery of mate choice.

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.

Temporal patterns of nutrition dependence in secondary sexual traits and their varying impacts on male mating success

Variation in the quantity of nutrients ingested over an individual's lifetime is likely to differentially affect distinct male secondary sexual traits and courtship signals, potentially providing females with information about a male's past and present foraging history. We hypothesize that female choice is thus influenced by a male's lifetime foraging history. To test this, we manipulated the quantity of nutrients (i.e. prey items) available to male wolf spiders, Schizocosa stridulans, using a fully crossed 2 × 2 design with low versus high prey quantity across juvenile and adult life stages, and assessed the impact of these diet treatments on male foreleg pigmentation, courtship rate and mating success. We found foreleg pigmentation to be dependent upon both juvenile and adult diet, with increased nutrition dependence of pigmented versus unpigmented leg segments. Despite this, the degree of foreleg pigmentation did not predict mating success. In contrast, courtship rate was not nutrient dependent, yet strongly predicted mating success. Finally, we found a significant interaction between juvenile diet, adult diet and courtship rate on mating success. Males that experienced a diet switch (low juvenile to high adult, LH; high juvenile to low adult, HL) exhibited no relationship between courtship rate and mating success, while those that experienced a consistent diet (LL; HH) showed increased mating success with increased courtship rates. Our results suggest that nutrition dependence of secondary sexual traits is not necessarily a predictor of their role in mating success and that female mate choice is the result of complex interactions between multiple male traits.

Fecundity selection does not vary along a large geographical cline of trait means in a passerine bird

Local environmental and ecological conditions are commonly expected to result in local adaptation, although there are few examples of variation in phenotypic selection across continent-wide spatial scales. We collected standardized data on selection with respect to the highly variable plumage coloration of pied flycatcher (Ficedula hypoleucaPall.) males from 17 populations across the species' breeding range. The observed selection on multiple male coloration traits via the annual number of fledged young was generally relatively weak. The main aim of the present study, however, was to examine whether the current directional selection estimates are associated with distance to the sympatric area with the collared flycatcher (Ficedula albicollisTemminck), a sister species with which the pied flycatcher is showing character displacement. This pattern was expected because plumage traits in male pied flycatchers are changing with the distance to these areas of sympatry. However, we did not find such a pattern in current selection on coloration. There were no associations between current directional selection on ornamentation and latitude or longitude either. Interestingly, current selection on coloration traits was not associated with the observed mean plumage traits of the populations. Thus, there do not appear to be geographical gradients in current directional fecundity selection on male plumage ornamentation. The results of the present study do not support the idea that constant patterns in directional fecundity selection would play a major role in the maintenance of coloration among populations in this species. By contrast, the tendency for relatively weak mosaic-like variation in selection among populations could reflect just a snapshot of temporally variable, potentially environment-dependent, selection, as suggested by other studies in this system. Such fine-grained variable selection coupled with gene flow could maintain extensive phenotypic variation across populations.(c) 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 808-827.

Mating success is predicted by the interplay between multiple male and female traits in the small hairy maggot blowfly

Intersexual selection drives the evolution of reproductive traits, including ornamentation and courtship behaviour. However, most studies attempting to explain the relationships between reproductive traits are oversimplified because traits are evaluated independently, and assessment of mate choice is restricted to one sex. Further research is required to understand the extent to which interactions between traits influence mating decisions in both sexes. The small hairy maggot blowfly, Chrysomya varipes, offers an ideal opportunity to examine how interactions between foreleg ornamentation (males have conspicuous white and black hairs, whereas females have only black hairs) and complex courtship behaviour influence mating success in males and females. This study involved mate choice trials between single females and males that varied in foreleg ornamentation. Courtship investment was quantified for males, and ornamentation and body size were quantified for both sexes. Mating success was predicted by time invested in courtship, but not by either male and female ornamentation or body size alone. However, there was a significant interaction between courtship investment, ornamentation and body size. At any given courtship investment, males with more ornamentation had an increased probability of mating success. Females with more ornamentation also had an increased probability of mating success, because males invested more courtship in more ornamented females. Furthermore, the lightest males had an increased probability of mating success compared to the heaviest males, as lighter males invested more in courtship. Female weight, however, did not significantly affect the probability of mating. The results suggest that male foreleg ornamentation in C. varipes acts as an amplifier of the visual courtship display, adding to a small but growing body of evidence that multiple male and female traits can interact to influence mating decisions.

EVOLUTION OF MALE COLORATION DURING A POST-PLEISTOCENE RADIATION OF BAHAMAS MOSQUITOFISH (GAMBUSIA HUBBSI)

Sexual signal evolution can be complex because multiple factors influence the production, transmission, and reception of sexual signals, as well as receivers' responses to them. To grasp the relative importance of these factors in generating signal diversity, we must simultaneously investigate multiple selective agents and signaling traits within a natural system. We use the model system of the radiation of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes to test the effects of resource availability, male body size and other life-history traits, key aspects of the transmission environment, sex ratio, and predation risk on variation in multiple male color traits. Consistent with previous work examining other traits in this system, several color traits have repeatedly diverged between predation regimes, exhibiting greater elaboration in the absence of predators. However, other factors proved influential as well, with variation in resource levels, body size, relative testes size, and background water color being especially important for several color traits. For one prominent signaling trait, orange dorsal fins, we further confirmed a genetic basis underlying population differences using a laboratory common-garden experiment. We illustrate a promising approach for gaining a detailed understanding of the many contributing factors in the evolution of multivariate sexual signals.

Selection on female remating interval is influenced by male sperm competition strategies and ejaculate characteristics

Female remating rate dictates the level of sperm competition in a population, and extensive research has focused on how sperm competition generates selection on male ejaculate allocation. Yet the way ejaculate allocation strategies in turn generate selection on female remating rates, which ultimately influence levels of sperm competition, has received much less consideration despite increasing evidence that both mating itself and ejaculate traits affect multiple components of female fitness. Here, we develop theory to examine how the effects of mating on female fertility, fecundity and mortality interact to generate selection on female remating rate. When males produce more fertile ejaculates, females are selected to mate less frequently, thus decreasing levels of sperm competition. This could in turn favour decreased male ejaculate allocation, which could subsequently lead to higher female remating. When remating simultaneously increases female fecundity and mortality, females are selected to mate more frequently, thus exacerbating sperm competition and favouring male traits that convey a competitive advantage even when harmful to female survival. While intuitive when considered separately, these predictions demonstrate the potential for complex coevolutionary dynamics between male ejaculate expenditure and female remating rate, and the correlated evolution of multiple male and female reproductive traits affecting mating, fertility and fecundity.

Female lizards discriminate between potential reproductive partners using multiple male traits when territory cues are absent

Female choice can powerfully influence the evolution of male phenotypes. In territorial species, it is challenging to determine the targets of female choice because male traits (e.g., behavior and morphology) are often correlated with territory. We sought to elucidate if and how females specifically evaluate male traits in a territorial species. In this study, we presented female fence lizards, Sceloporus undulatus, with two potential mates to examine mate choice in the absence of territory cues. Females associated more with males possessing better body condition, longer heads, and wider throat badges, and that performed more shudder behavior, which females responded to by approaching shuddering males and performing push-ups. A post hoc decision tree analysis suggests that the strongest predictor of female association was an overall quality index that incorporates all of these traits, rather than individual traits. Male snout–vent length, head width, abdominal badge width, and push-up behavior did not affect female association. Further research on why these traits, which are known to correlate with fitness, do not appear to be used by females when selecting mates would improve our understanding of the evolution of male traits. Our study reveals that females of this territorial species possess the ability to use multiple male traits interactively to make fitness-relevant mate choice decisions in the absence of direct territory cues.

Multiple signals in the palmate newt: ornaments help when courting

There is increasing evidence that female mate choice is often based on the assessment of multiple male traits, involving both morphology and behavior. We investigated female mate choice for multiple male traits in the palmate newt, Lissotriton helveticus, including male tail filament length, hind foot web size, crest development, body size, ventral coloration, and courtship display activity. Observations of courtship display in the field revealed that females spent more time in front of males with longer tail filaments. Laboratory experiments revealed a more detailed relationship between filament length and courtship display. We found that females took more sperm masses from males with both longer filaments and greater display activity. Experimental shortening of the tail filament length substantially decreased the number of male sperm masses transferred. However, when we experimentally reversed relative filament length between two males in mating trials, male mating success was explained by courtship activity and not by filament length. Our results show that female palmate newts value multiple traits during mate choice, including both morphological ornaments and reproductive behaviors in males. Our results further suggest that, when filament length is below a certain threshold, females may value the information content of courtship activity over that of filament length.

The effect of claw size and wave rate on female choice in a fiddler crab

How do females select a mate when they have mating preferences for multiple male traits? In experimental studies, female fiddler crabs (Uca mjoebergi) show a strong preference for males with larger claws and higher wave rates. In the field, there is no correlation between male claw size and observed wave rate. Here we document natural mating behaviour and show that females approach males who wave at a higher rate than nearby competitors. On average, an approached male had a significantly larger claw than his two nearest neighbours but did not differ in size from his two closest waving competitors. In general, smaller males were less likely to wave at approaching females. Females therefore approached mates based directly on wave rate but, because smaller males were less likely to wave, this indirectly resulted in female choice for larger than average males. Our study raises two issues. First, how do we relate the field results to previous experimental studies showing a female preference for larger claws? Second, in U. mjoebergi, males defend smaller neighbours against intruders. Our study suggests that one benefit of such defence coalitions is to decrease the number of immediate competitors present during female mate choice by retaining smaller neighbours.

SEXUAL SELECTION AND THE EVOLUTION OF GENITAL SHAPE AND COMPLEXITY IN WATER STRIDERS

Animal genitalia show two striking but incompletely understood evolutionary trends: a great evolutionary divergence in the shape of genitalic structures, and characteristic structural complexity. Both features are thought to result from sexual selection, but explicit comparative tests are hampered by the fact that it is difficult to quantify both morphological complexity and divergence in shape. We undertake a comparative study of multiple nongenitalic and male genital traits in a clade of 15 water strider species to quantify complexity and shape divergence. We show that genital structures are more complex and their shape more divergent among species than nongenital traits. Further, intromittent genital traits are more complex and have evolved more divergently than nonintromittent genital traits. More importantly, shape and complexity of nonintromittent genital traits show correlated evolution with indices of premating sexual selection and intromittent genital traits with postmating sexual selection, suggesting that the evolution of different components of genital morphology are shaped independently by distinct forms of sexual selection. Our quantitative results provide direct comparative support for the hypothesis that sexual selection is associated with morphological complexity in genitalic traits and highlight the importance of quantifying morphological shape and complexity, rather than size in studies of genital evolution.

Effects of sensory modality on learned mate preferences in female swordtails

Females often base their mate selection on multiple male traits. Different cues may be weighted differently in mating decisions, and play different roles such as indicating species identity or condition. The ontogeny of preferences for each cue can differ, which may offer a proximate explanation for the differential female evaluation of multimodal traits of males. We investigated whether female preferences for the multimodal male cues of Xiphophorus birchmanni swordtails are learned for traits in both olfactory and visual sensory modalities. We reared X. birchmanni females with either conspecific adults or adults of a closely related species, Xiphophorus malinche. We found that both olfactory and visual preferences were learned, and that the timing of olfactory learning was different from that of visual cues. (C) 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. (Less)

Female Choice for Males with Greater Fertilization Success in the Swedish Moor Frog, Rana arvalis

BackgroundStudies of mate choice in anuran amphibians have shown female preference for a wide range of male traits despite females gaining no direct resources from males (i.e. non-resource based mating system). Nevertheless, theoretical and empirical studies have shown that females may still gain indirect genetic benefits from choosing males of higher genetic quality and thereby increase their reproductive success.Methodology/Principal FindingsWe investigated two components of sexual selection in the Moor frog (Rana arvalis), pre-copulatory female choice between two males of different size (‘large’ vs. ‘small’), and their fertilization success in sperm competition and in isolation. Females' showed no significant preference for male size (13 small and six large male preferences) but associated preferentially with the male that subsequently was the most successful at fertilizing her eggs in isolation. Siring success of males in competitive fertilizations was unrelated to genetic similarity with the female and we detected no effect of sperm viability on fertilization success. There was, however, a strong positive association between a male's innate fertilization ability with a female and his siring success in sperm competition. We also detected a strong negative effect of a male's thumb length on his competitive siring success.Conclusions/SignificanceOur results show that females show no preference for male size but are still able to choose males which have greater fertilization success. Genetic similarity and differences in the proportion of viable sperm within a males ejaculate do not appear to affect siring success. These results could be explained through pre- and/or postcopulatory choice for genetic benefits and suggest that females are able to perceive the genetic quality of males, possibly basing their choice on multiple phenotypic male traits.

Effects of egg testosterone on female mate choice and male sexual behavior in the pheasant

Evidence is accumulating that sex steroids in the eggs, besides affecting progeny phenotype and behavior in the short term, also have enduring effects until adulthood, when they may translate into differences in reproductive strategies and success. Maternal steroids transfer may therefore affect both agonistic behavior and mate choice decisions, either through the promotion of body size and condition or through a priming effect on the neuroendocrine system. However, owing to the prevalence of a short-term perspective, relevance of maternal transfer of sex steroids to sexual selection processes has been seldom studied. Here we investigate the effects of an experimental increase in egg testosterone on male dominance and copulation success in the ring-necked pheasant, Phasianus colchicus, a polygynous galliform with multiple male ornamental traits, in captivity. We found that females from testosterone (T) injected eggs copulated less than control females. Males from T-injected eggs obtained more copulations than control males, specifically with control females. The effect of male ‘ordinary’ and secondary sexual traits on either dominance or copulation frequency did not depend on early exposure to T, nor did T treatment affect male dominance. Present results demonstrate that variation in the early hormonal environment set up by mothers affects sexual behavior of the offspring, which might translate into fitness differences.

Distinguishing between male and territory quality: females choose multiple traits in the pied flycatcher

To understand how sexual selection works, it is important to distinguish between the mechanisms underlying mating success. One of the basic questions is to differentiate between the importance of territory-related resources (gained through male–male competition) and male quality in female choice. Few studies, however, have tried to separate these two often intercorrelated variables. We randomized territory quality among male pied flycatchers, Ficedula hypoleuca, and studied which male traits were associated with their success in female mate choice. Females appeared to choose multiple male traits in the wild when the males were not allowed to choose territories before female choice for males. Males with a long tarsus, large white wing patch and versatile song were favoured by females. In addition, the contrast of ultraviolet (UV) reflectance in the white wing patch relative to its background, that is, the dorsal brown-black coloration of the males, appeared to be an important mate choice cue. The UV reflectance had a stronger effect on pairing success in dark males than in brown ones. An experimental manipulation of the UV reflectance revealed that the UV coloration of the males appeared to be used in female choice early but not late in the pairing season, which suggests time-dependent plasticity in female choice. Our study thus exemplifies the complexity of mate choice; it is both temporally constrained and dependent on multiple ornaments.

Experience counts: females favor multiply mated males over chemically endowed virgins in a moth (Utetheisa ornatrix)

Determining the factors that affect male mating success is essential to understanding how sexual selection operates, including explanations of the adaptive value of female preferences and how variation in male traits is maintained in a population. Although females may appear to choose males based on a single parameter, female mate choice is often a complex series of assessments of male quality that can only be revealed through manipulation of multiple male traits. In the moth Utetheisa ornatrix (Lepidoptera: Arctiidae), females have been shown to judge males primarily on their production of a courtship pheromone, hydroxydanaidal, derived from defensive chemicals acquired as larvae. Recent work, however, suggested that other factors, including prior mating experience by males, may also influence the outcome of precopulatory interactions with females. I ran mating trials with one female and two males to determine whether there were any differences in male mating success based on their prior exposure to females, mating experience, and time between matings. Previously mated males were favored over virgins when both males lacked the pheromone, but courting experience and mating interval did not explain these differences in male mating success. Furthermore, multiply mated males lacking the pheromone were favored over virgin males that produced the pheromone, thus reversing the commonly observed trend of female precopulatory bias towards males with higher levels of the pheromone. These results demonstrate that males with mating experience can secure copulations despite deficiencies in the pheromone, and I provide possible mechanisms and discuss their implications regarding sexual selection.

Female choice for optimal combinations of multiple male display traits increases offspring survival

Females commonly incorporate information from more than 1 male trait when making mating decisions, which may increase their ability to choose high-quality males. Assessment of multiple male traits may also incur increasing costs of time and/or energy and should therefore provide an adaptive advantage over females that do not exhibit such complex mating decisions. Although this benefit has been assumed/concluded in previous mate choice studies, it has rarely been empirically verified with female fitness data. Here we show that female side-blotched lizards (Uta stansburiana) that assess males for optimal trait combinations of throat color (a polymorphic social signal) and dorsal patterning (a polymorphic antipredator trait) recruit more offspring to the next adult generation. Specifically, females preferred males with a barred dorsal pattern, but only when males were yellow throated (signaling a sneaker strategy in males). Females mated to sires with both these traits experienced high rates of progeny survival to adulthood, via inheritance of favorable genetic combinations from sires (indirect benefits). Previous results suggest that this is because barredness confers crypsis primarily in yellow-throated lizards and not in lizards with alternative throat colors. Together, these results support the hypothesis that female preference for multiple, interacting male traits is an adaptive response to complex patterns of natural selection on offspring, such as correlational selection on unlinked traits. Our results provide new evidence for an adaptive advantage to females that exhibit complex mating-decision rules and suggest that one advantage lies in reducing deleterious recombination of genes for traits that, only in specific combinations, enhance fitness. Key words: alternative strategies, color pattern polymorphism, correlational selection, crypsis, good genes sexual selection, indirect benefits, multivariate signaling (multicomponent display). [Behav Ecol]