The Allure of the Distinctive: Reduced Sexual Responsiveness of Female Guppies to 'Redundant' Male Colour Patterns

Frequency-dependent mating behaviour has the potential to maintain genetic variation in characteristics of organisms. The colour patterns of guppies ( Poecilia reticulata ) provide an example of one of the most extreme genetically based polymorphisms known in nature, for which frequency-dependent mate choice could be a mechanism. Numerous studies have shown that female guppies base mating preferences on male colour patterns and there is evidence that females prefer to mate with males displaying novel or unfamiliar colour patterns. This preference could lead to frequency-dependent mating success in males. Nevertheless, the possibility that female sexual responsiveness itself may depend on the frequency of male types has not been tested systematically in guppies or any other species. This study examined the sexual responses of female guppies in experimental groups consisting of two males with similar (redundant) and two males with different (unique) colour patterns. We found that female guppies were much more likely to respond sexually to the displays of unique males than to those of redundant males. Further, there was no effect of orange colouration on female responsiveness as has been documented for this population in several previous studies, thus, discrimination against redundant male types appears to have overridden directional selection based on colour pattern characteristics. This discrimination against redundant male types could in turn lead to frequency-dependent mating success in males and maintenance of colour pattern polymorphism.     

Scent marking and mate choice in the prairie vole, Microtus ochrogaster

Scent marking is common among male and female rodents and might be used in male-male competition and as a mechanism for mate attraction. I tested the hypotheses that females would choose males based on their frequency and placement of scent marks, and that a female would advertise interest in a particular male by placing her scent marks on or near those of a preferred mating partner. In a series of experiments conducted with prairie voles, Microtus ochrogaster, females did not choose mates based on the frequency or placement of scent marks by males nor did they advertise their interest in a particular male through the frequency or placement of scent marks. The number of males chosen that scent-marked more than their opponents did not differ significantly between females exposed (11 of 15) and not exposed (10 of 15) to scents of males. Females exposed and not exposed to scents of males preferred seven of the same males that had scent-marked more than their opponents. When a third group of females was exposed to four times more scent of the less preferred than preferred males, they still chose the preferred males. Thus, the frequency and placement of scent marks by males were not used to assess males for mate choice nor did female prairie voles use scent to advertise their preference for a mating partner. In that scent marking is common in male and female mammals, scent quality might be more important than quantity in male-male competition and mate attraction.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Effects of tapeworm infection on male reproductive success and mating vigor in the red flour beetle,Tribolium castaneum

Parasites may exert negative effects on host survivorship and reproductive success. The effects of parasites on female host fitness have been well documented; however, the effects of parasites on the reproductive success of male hosts and particularly the underlying mechanisms that alter male fitness are not well understood. Previous studies demonstrated that infection by rat tapeworm (Hymenolepis diminuta) reduced the fitness of male red flour beetles (Tribolium castaneum) in an environment of female mate choice and strong male-male competition. The present study determined the role of female mate choice and male insemination capacity on observed fitness reduction of male beetles by the tapeworm parasites. We found that infected males showed reduced mating vigor and consequently inseminated fewer females than did uninfected males. Specifically, tapeworm infection reduced the number of offspring sired by a male by 14-22% even when male-male competition and female mate choice were absent. Further, the insemination capacity of males diminished by 30% because of infection. Female beetles did not discriminate against infected males in precopulatory mate choice experiments. Copulatory courtship, a determinant of postcopulatory female choice, was not significantly different between infected and uninfected males. Hence, we concluded that female beetles did not show either pre- or postcopulatory choice against tapeworm-infected males. Therefore, tapeworm-induced reduction in the reproductive success of male beetles possibly results from altered reproductive biology, such as lower mating vigor and decreased sperm quantity or quality.     

Male-male interactions and their influence on the mating behavior and success in the fountain darter, <Emphasis Type="Italic">Etheostoma fonticola</Emphasis>

Behavioral interactions between individuals of the same sex can affect the outcome of intersexual selection. For this reason, intrasexual selection is oftentimes examined independently from intersexual selection in studies aimed at understanding mating behaviors. However, a more complete understanding of sexual selection effects within a population can only come from exploring both intrasexual and intersexual selection and the potential interactions between the levels of selection. Association preferences in male and female Etheostoma fonticola do not reveal a size preference for same sex or opposite-sex individuals. However, male-male interactions may influence female choice in E. fonticola. We examined whether male E. fonticola that differ in body size exhibit differences in agonistic behaviors and mating success. Larger males do exhibit higher rates of aggressive behaviors and smaller males, in turn, exhibit more defensive behaviors. However, differences between larger and smaller males in male-male interactions did not translate into differences in spawning success. These results suggest that male size influences dominance relationships in E. fonticola but not mating success. There were also no differences between large and small males in mating attempts, which could be an outcome of the year-round breeding season found in this species, females laying eggs singly, or males fertilizing eggs individually.     

Path analysis and the relative importance of male-female conflict, female choice and male-male competition in water striders

Three major behavioural mechanisms underlying sexual selection in many systems are male-male competition, female choice and male-female conflict. We used path analysis to evaluate the relative importance of these mechanisms in generating sexual selection on a suite of male traits in the stream-dwelling water strider, Aquarius remigis. To gather data for the analysis, we quantified the morphology (total length, limb length, forefemur width, genital length), behaviour (activity), mating frequency, mean mating duration and overall mating success of 96 adult males over a 10-day period. Males varied considerably in mating success. Over the 10 days, individual males mated 0-14 times, spending 0-67% of their time in copula. Path analysis showed that male-male competition was important in favouring larger males with longer limbs that tended to be more active. Active males should encounter females more frequently. In water striders, almost all male-female encounters result in intense premating struggles pitting female resistance to mating against male insistence. This male-female conflict favoured larger males with longer genitalia. These traits help males overcome female resistance. Female choice was expressed via female-controlled variation in mate-guarding durations. Female choice favoured smaller males perhaps because they are lighter, less expensive ‘shields’ against harassment by other males. Male size thus affected mating success via all three behavioural mechanisms. Weak, overall sexual selection favouring larger males was the product of conflicting effects: male-female conflict strongly favouring larger males and male-male competition weakly favouring larger males, offset by female choice favouring smaller males. Separate analyses for warmer versus colder days showed that on colder days (daily high below 20 °C), male-male competition was the main mechanism generating variation in mating frequency, while on warmer days, both male-male competition and male-female conflict were important. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Why do multiple traits determine mating success? Differential use in female choice and male competition in a water boatman

Mating success is often determined by multiple traits, but why this occurs is largely unknown. Much attention has been paid to female preferences for multiple traits, but surprisingly few researchers have addressed the possibility that multiple traits are important because they serve different functions in female choice and male-male competition. Differential trait function could result from a conflict of interest between the sexes or from constraints forcing the sexes to pay attention to different traits. I show that traits determined at distinct life-history stages differ in their importance in female choice and male-male competition in a water boatman Sigara falleni. Juvenile conditions determined body and foreleg pala size and were the main determinants of mating success under female choice, whereas adult conditions determined body mass and influenced mating success when male competition was included. This differential use of condition-dependent traits under the two selection regimes appeared to arise partly from a conflict between the sexes, since the two selection forces (female choice and male competition) conflict for selection on pala size, and partly from constraints, as females appeared unable to assess adult condition.     

Sexual selection for male dominance reduces opportunities for female mate choice in the European bitterling (Rhodeus sericeus)

Sexual selection involves two main mechanisms: intrasexual competition for mates and intersexual mate choice. We experimentally separated intrasexual (male-male interference competition) and intersexual (female choice) components of sexual selection in a freshwater fish, the European bitterling (Rhodeus sericeus). We compared the roles of multiple morphological and behavioural traits in male success in both components of sexual competition, and their relation to male reproductive success, measured as paternity of offspring. Body size was important for both female choice and male-male competition, though females also preferred males that courted more vigorously. However, dominant males often monopolized females regardless of female preference. Subordinate males were not excluded from reproduction and sired some offspring, possibly through sneaked ejaculations. Male dominance and a greater intensity of carotenoid-based red colouration in their iris were the best predictors of male reproductive success. The extent of red iris colouration and parasite load did not have significant effects on female choice, male dominance or male reproductive success. No effect of parasite load on the expression of red eye colouration was detected, though this may have been due to low parasite prevalence in males overall. In conclusion, we showed that even though larger body size was favoured in both intersexual and intrasexual selection, male-male interference competition reduced opportunities for female choice. Females, despite being choosy, had limited control over the paternity of their offspring. Our study highlights the need for reliable measures of male reproductive success in studies of sexual selection.     

Female sand gobies prefer good fathers over dominant males

Female preference for males successful in male-male competition is generally assumed to result in mating with high quality males. Here I report results from an experiment disentangling the effects of intra- and intersexual selection in the sand goby, Pomatoschistus minutus, a marine fish that exhibits paternal care. I show that large males are successful in male–male competition, but contrary to what one would expect, dominants are not preferred by females and are not better at taking care of the eggs. Female preference, however, correlated with the subsequent hatching success of the eggs. Thus, female choice selects for good parenting. Hence, direct benefits in the form of superior paternal care can explain female choice in this species, supporting a good parent process of sexual selection. However, choosing on the outcome of male–male competition does not enable females to mate with the ''best'' males.     

Superior fighters make mediocre fathers in the Pacific blue-eye fish

It is widely assumed that male competition and female choice select for elaboration of the same male traits and that fighting ability is synonymous with high quality in terms of benefits to females. Under these assumptions, females are expected to use the same traits that reflect fighting ability to choose the most dominant male, even if females are not privy to actual male-male interactions. Few studies, however, have explicitly investigated female choice in relation to male fighting ability. I conducted experiments separating the effects of male competition and female choice in a freshwater fish, the Pacific blue-eye, Pseudomugil signifer, to test whether females prefer dominant males and whether females obtain higher egg hatching success by being choosy. When females were precluded from witnessing agonistic encounters between two potential mates, they did not appear to use traits correlated with fighting ability to choose competitively superior males. However, even when females were privy to competition, witnessing male interactions did not induce a preference for dominant individuals. Lack of preference for superior fighters may be because there was no difference in hatching success between eggs guarded by dominant and subordinate males. Instead, females appeared to prefer males that spent a greater proportion of time engaged in courtship and, in so choosing, enjoyed higher egg hatching success. These results indicate that dominant males are not necessarily more attractive than subordinates nor do the former necessarily guarantee or deliver the kind of benefits that females may seek.     

Female choice, male interference, and sperm precedence in the red-spotted newt

Darwin first identified female choice and male—male competitionas forms of sexual selection resulting in the evolution of conspicuoussexual dimorphism, but it has proven challenging to separatetheir effects. Their effects on sexual selection become evenmore complicated when sperm competition occurs because spermprecedence may be either a form of cryptic female choice ora form of male—male competition. We examined the effectsof tail height on male—male competition and female choiceusing the sexually dimorphic red-spotted newt (Notophthalmusviridescens viridescens). Experiment 1 examined whether maletail height influenced male mating success. Males with deeptails were more successful at mating with females than thosewith shallow tails. Successful, deep-tailed males also were bigger(snout-vent length; SVL) than unsuccessful, shallow-tailed males,but they did not vary in tail length or body condition. Of these,only tail height and tail length are sexually dimorphic traits.Experiment 2 tested the hypothesis that the differential successof males with deeper tails was due to female choice by examiningboth simultaneous female preference for association and sequentialfemale choice. We found no evidence of female choice. When maleswere not competing to mate with females, tail height did notinfluence male mating success. Successful males did not havedifferent SVL and tail lengths than unsuccessful males. Thus,tail height in male red-spotted newts appears to be an intrasexuallyselected secondary sexual characteristic. Experiment 3 usedpaternity exclusion analyses based on molecular genetic markersto examine the effect of sperm precedence on sperm competitionin doubly-mated females. Sperm precedence likely does not havea pervasive and consistent effect on fertilization success becausewe found evidence of first, last, and mixed sperm usage.     

Geographic variation in the function of ornaments in the common yellowthroat Geothlypis trichas

We used controlled aviary experiments to study the role of male ornaments in male-male competition and female choice in the common yellowthroat Geothlypis trichas , a sexually dichromatic warbler. Previous aviary studies in Wisconsin, USA, indicated that males with larger black facial masks were dominant over males with smaller masks and preferred by females in mate choice experiments. In this study, we replicated those experiments in a population in New York, USA, where male mating success was related more consistently to the size of the yellow bib (throat, breast, and belly) than to the size of the mask. Similar to the study in Wisconsin, we found that males with larger masks were more likely to be dominant in New York, however, we found that males with larger bibs were preferred by females in New York, and there was no significant preference for males with larger masks. These results are consistent with the hypothesis that carotenoid-based ornaments are selected by female choice and melanin-based ornaments are selected by male-male competition. However, the pattern of female choice appears to vary between New York and Wisconsin. This geographic difference could be related to a variety of environmental factors (habitat, carotenoid and parasite abundance) that affect the costs and benefits of choosing males with particular ornaments in each location.     

DOES LARGE BODY SIZE IN MALES EVOLVE TO FACILITATE FORCIBLE INSEMINATION? A STUDY ON GARTER SNAKES

A trend for larger males to obtain a disproportionately high number of matings, as occurs in many animal populations, typically is attributed either to female choice or success in male-male rivalry; an alternative mechanism, that larger males are better able to coercively inseminate females, has received much less attention. For example, previous studies on garter snakes (Thamnophis sirtalis parietalis) at communal dens in Manitoba have shown that the mating benefit to larger body size in males is due to size-dependent advantages in male-male rivalry. However, this previous work ignored the possibility that larger males may obtain more matings because of male-female interactions. In staged trials within outdoor arenas, larger body size enhanced male mating success regardless of whether a rival male was present. The mechanism involved was coercion rather than female choice, because mating occurred most often (and soonest) in females that were least able to resist courtship-induced hypoxic stress. Males do physically displace rivals from optimal positions in the mating ball, and larger males are better able to resist such displacement. Nonetheless, larger body size enhances male mating success even in the absence of such male-male interactions. Thus, even in mating systems where males compete physically and where larger body size confers a significant advantage in male-male competition, the actual selective force for larger body size in males may relate to forcible insemination of unreceptive females. Experimental studies are needed to determine whether the same situation occurs in other organisms in which body-size advantages have been attributed to male-male rather than male-female interactions.     

Cryptic female choice in the yellow dung fly Scathophaga stercoraria (L.)

Both female choice and male-male competition may take place during reproduction in many species. Female choice tends to be less obvious than male-male competition and consequently has received less attention from researchers. The opportunity for cryptic female choice arises after multiple insemination. Through postcopulatory processes, a female could alter the pattern of paternity among her offspring so that it does not directly reflect the different contributions of sperm made by her mates. To be able to determine if a female alters the relative sperm contributions of her mates, the behaviors and influences of the males must therefore be first taken into account. The interest of each male is to father all the offspring, and the interest of each female is to maximize paternal quality. Female yellow dung flies have complex internal reproductive tracts that may give them considerable control over the fertilization success of stored sperm from different males. In laboratory trials to date, the last male to mate has usually been most successful. In the present study, cryptic choice occurred in Scathophaga stercoraria and the pattern of choice was consistent with previously reported results. The fertilization success of a female's second mate (P2) was substantially larger if a female was kept at constant temperature and if the second male was genetically similar to her at the phosphoglucomutase (Pgm) locus. Females from the field normally have three spermathecae, but some have four. Lines were bred to have either three or four spermathecae. Flies from the different lines were crossed to generate females with similar genetic backgrounds that had either three or four spermathecae. P2 was significantly lower for high-quality females, that is, those that laid larger-than-average-clutches, with four spermathecae than for low-quality females with four spermathecae; female quality had no influence on P2 for females with three spermathecae. The results suggest that only large females may benefit from increased spermathecae number by being able to act against male interests. Females may only have three spermathecae, even though genetic variation for more is present, because selection for more spermathecae is weak.     

Population density influences male-male competition in guppies

This study tested the general prediction that population density affects male-male competition, female mate choice and the opportunity for sexual selection. By manipulating the density of guppies, Poecilia reticulata, while keeping the sex ratio constant, I found that male mating tactics were phenotypically plastic with respect to density. As density increased, males decreased their courtship displays. Male-male competition and mate searching were highest at intermediate densities. Population density had no significant effect on the total number of copulations, copulatory tactics or the percentage of postcopulatory guarding. Female preference for males with a higher percentage of orange coloration was similar at all density levels. The 'opportunity for sexual selection', which estimates the upper limit to which a selected trait can shift if directional selection is operating and was calculated as the variance in number of copulations per male divided by the square of the mean number of copulations, was negatively associated with population density. This may be due to the decrease in male-male competition at high density rather than female preference which was similar across density treatments. Copyright 1999 The Association for the Study of Animal Behaviour.     

The role of female dominance hierarchies in the mating behaviour of mosquitofish

While studies of sexual selection focus primarily on female choice and male-male competition, males should also exert mate choice in order to maximize their reproductive success. We examined male mate choice in mosquitofish, Gambusia holbrooki, with respect to female size and female dominance. We found that the number of mating attempts made by a male was predicted by the dominance rank of females in a group, with dominant females attracting more mating attempts than subordinates. The number of mating attempts made by males was independent of the female size. The observed bias in the number of mating attempts towards dominant females may be driven either by straightforward male mate choice, since dominance and female fecundity are often closely related, or via the dominant females mediating male mating behaviour by restricting their access to subordinate females.     

Reproductive strategies of rhesus macaques

Reproductive strategies incorporate a multitude of mechanisms that have evolved to promote the reproductive success of individuals. Evolutionary perspectives tend to emphasize the advantages of male-male competition and female choice as mediators of differential reproduction. Male rhesus macaques have not been observed to fight for access to sexually receptive females, although they suffer more wounds during the mating season. An increased likelihood of attacks appears to coincide with male troop entry. Males who spend more time in consort and mate with more females tend to sire more offspring. Genetic analysis of paternity has pinpointed age and endurance rivalry, rather than agonistic competition, as key variables associated with variation in progeny production. Female rhesus macaques often copulate with multiple males during their ovulatory period, and tend to conceive on the first cycle of the mating season. Female reproductive success is more likely to be a function of offspring survivorship than the identity of particular male partners. The role of female choice as a direct mediator of male reproductive success is unresolved, but female mate selection seems to indirectly affect male reproductive success because female preference for mating with novel males seems to foster male dispersal. Evaluating whether mating preferences for particular male phenotypes affectsfemale reproductive success is a task for the future. A common denominator to the reproductive strategies of both female and male rhesus macaques is that feeding patterns affect body condition which influences reproductive output and regulates relative reproductive success.     

Female choice for males with greater fertilization success in the Swedish Moor frog, Rana arvalis

Background

Studies 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 Findings

We 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/Significance

Our 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.     

Ultraviolet nuptial colour determines fight success in male European green lizards (Lacerta viridis)

Animal communication through colour signals is a central theme in sexual selection. Structural colours can be just as costly and honest signals as pigment-based colours. Ultraviolet (UV) is a structural colour that can be important both in intrasexual competition and mate choice. However, it is still unknown if a UV signal alone can determine the outcome of male-male fights. European green lizard (Lacerta viridis) males develop a nuptial throat coloration with a strong UV component. Among males differing only in their manipulated UV colour, females prefer males with higher UV. Here, we experimentally decreased the UV coloration of randomly chosen males from otherwise similar male pairs to test the hypothesis that a difference in UV colour alone can affect fight success during male-male competition. Our results fully supported the hypotheses: in almost 90 per cent of the contests the male with reduced UV lost the fight. Our results show that UV can be an important signal, affecting both female mate choice and determining male fight success.     

Sexual selection in an anadromous population of threespine sticklebacks — no role for parasites

Summary We examined the hypothesis that trematode parasites played a role in the evolution of the red colour of male threespine sticklebacks (Gasterosteus aculeatus L.) and whether the parasites affected female fitness. Parasites (blackspot disease) played no role either in determining the outcome of male—male competition for breeding territories or in female mate choice. Among males with territories, mating success was highly variable. Some males obtained over 3000 eggs (approximately 10 matings) whereas others received none. In 1 year of the 2 year study, males with the greatest amount of red nuptial coloration had the greatest mating success. Although male colour may sometimes affect female choice in this system, this preference has probably not evolved because of the Hamilton—Zuk mechanism of sexual selection. The parasites had small, but statistically significant effects on female fitness. Females with high parasite loads were in poorer condition and produced fewer eggs than less parasitized fish.