Females decide whether size matters: plastic mate preferences tuned to the intensity of male-male competition

Recent studies have indicated that mating success of large malesmay improve under increasing levels of mating competition. Thisoutcome is explained 1) if male mating competition is overridingfemale preferences for male traits that are unrelated to, ornegatively correlated with, male size and dominance and, inso doing, dictates the distribution of matings or 2) if femalesalter their preferences with respect to large males when male–malecompetition is intense. Under both hypotheses, one could expectlarge, dominant males to be more successful under intense competitionthan under weak competition. However, only the first explanationpredicts that male mating success under intense competitionshould be determined by dominance; traits that are unrelatedto male dominance should be uncorrelated to mating success.In contrast, if females change their preferences (explanation2), males with traits beneficial to females independent of thecompetitive environment can maintain a high mating success underall levels of male–male competition. We tested these alternativesusing a small marine fish, the sand goby, Pomatoschistus minutus.The mating success of large males increased under conditionsallowing intense male competition, whereas females showed apreference for good nest building independent of the level ofcompetition. These findings suggest that females are in controlof their choice by altering their preference for male size inresponse to the intensity of male–male competition ratherthan female preference being overshadowed by male dominance.This plasticity of preferences implies that the strength ofsexual selection is not constant at the population level.     

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.     

Mating preference of female zebrafish, Danio rerio, in relation to male dominance

Mating success tends to be skewed toward dominant males, thoughfemale mate preferences may not always correlate with male dominance.In this study, we investigated the mating preferences of femalezebrafish, Danio rerio, in the absence of male–male competition.We paired females sequentially with males of known dominancerank, using a nested, repeated measures design, with egg productionas a measure of female mate preference. We predicted that femaleswould spawn more frequently and produce larger clutches whenpaired with males of higher dominance rank. We found significantdifferences among females in the size of clutches produced andamong males in the size of clutches received, but these differenceswere independent of male dominance rank. Male body size wasnot related to either dominance rank or clutch size received.These results indicate that females vary clutch size in relationto the males with which they are paired but that they do notfavor dominant males. Thus, male competition may normally overridefemale mate preference in zebrafish.     

Should females prefer dominant males?

It is generally believed that success in male–male competition genuinely reflects high quality and that female preference for dominant males should therefore be widespread. However, recent studies suggest that male dominance is not always attractive and that it does not necessarily predict superior parental quality, better genes or other forms of benefit to females. In fact, the costs of choosing a dominant male can sometimes outweigh the benefits. When traits selected by male–male competition do not reflect overall mate quality, females are expected to use other choice cues and might occasionally prefer subordinate males. Thus, male–male competition and female choice can sometimes work in different, or even opposing, directions.     

Male pipefish prefer dominant over attractive females

Animals may obtain information guiding their choice betweenpotential partners from observing competitive interactionsand displays between them, or from displays directed at thechoosing individual. In the sex-role reversed pipefish Syngnathustyphle females display a temporary ornament (a color pattern)to other females as well as to males. We have previously shown that display of female ornaments per se is attractive to males.Here we show that information from competitive displays canoverride such direct attraction displays as signals in thepartner choice process. In a mate choice experiment, an enclosedmale could choose between two females. On the first experimentalday, females could interact freely, while on the second daythey were isolated from each other. When female-female competitionwas allowed, the ornament display was directed more to theother female than to the male: Time competing, rather thantime courting the male, correlated with ornament display duration.However, ornament display under competition and ornament displayin the absence of competition did not correlate significantly.In fact, females competing more intensively on day one displayedthe ornament less on day two. Furthermore, the ornament displayduring the first, but not the second, day predicted male matechoice on the second day. Thus, males remembered previous informationfrom competitive displays and used it rather than immediateinformation from displays in the absence of female-female competition.We suggest that competitive displays more reliably signal female quality as compared to noncompetitive ones, and that males benefitfrom mating with dominant females.     

Treat ’em Mean,Keep ’em (sometimes) Keen: Evolution of Female Preferences for Dominant and Coercive Males

How should females choose their mates if choice is not completely free, but at least partly dictated by outcomes of male–male competition, or sexual coercion? This question is of central importance when evaluating the relationship between sexually antagonistic ‘chase-away’ scenarios and models of more traditional female choice. Currently, there is a mismatch between theories: indirect benefits are seen to play a role in conventional mate choice, whereas they are not predicted to have an influence on the outcome if matings impose direct costs on females. This is at odds with the idea that resistance and preference are two sides of the same coin: either leads to a subset of males enjoying enhanced mating success. In the same way as choosy females benefit from mating with sexy males if this yields sexy sons, females could benefit from being manipulated or ‘seduced’, if the manipulative or seductive ability of males is heritable. Here I build a model where male dominance (or coerciveness) improves his mating success, and this relationship can be modified by female behaviour. This clarifies the definitions of resistance and preference: resisting females diminish the benefit a male gains from being dominant, while preferences enhance this pre-existing benefit enjoyed by dominant males. In keeping with earlier theory, females may evolve to resist costly mating attempts as a counterstrategy to male traits, particularly if male dominance is environmentally rather than genetically determined. Contrary to earlier results, however, indirect benefits are also predicted to influence female mating behaviour, and if sufficiently strong, they may produce female preferences for males that harm them.     

Sexual selection in a moth: effect of symmetry on male mating success in the wild

Sexual selection is generally caused by female choice and male–malecompetition. In female choice process, female preference isfavored indirectly and/or directly by sexual selection. In indirectselection, females expressing the preference might gain indirectgenetic benefits. In direct selection, females expressing thepreference might gain direct benefits or avoid male-imposedcosts. The white-tailed zygaenid moth Elcysma westwoodii ismonandrous, and males often gather around a female to mate withher, suggesting a high opportunity for sexual selection on maletraits. We quantified phenotypic selection on male morphologyin this species in the field. The morphological characters analyzedincluded body weight, antenna length, forewing length, hindwing length, hind wing tail length, genital clasper length,and the fluctuating asymmetry (FA) of these bilateral traits.In E. westwoodii, selection favored males with more symmetricgenital claspers, as well as longer and more symmetrical hindwings and antennae. Negative correlations between FA and sizewere also detected in the clasper and the antenna. Our resultssuggest that FAs of male traits, in particular the genital clasper,may have indirect and direct influences on mating success. Duringa copulatory attempt, an E. westwoodii male will try to graspthe female's abdominal tip with his claspers but often failto do so because of the female's reluctance to mate. The femaleabdominal tips are smooth and strongly sclerotized and couldthus be difficult for males to grasp. We hypothesize that moresymmetrical male claspers are more efficient in overcoming femalereluctance.     

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.     

Mate copying versus preference for actively courting males by female Japanese medaka (Oryzias latipes)

We determined whether female Japanese medaka (Oryzias laiipes)copied the choice of other females or independently preferredactively courting males. We allowed focal females to observeand subsequently choose between a male that courted and potentiallyspawned with a receptive female and a male that courted andwas rejected by an unreceptive female. When the receptive femaledid not spawn, the focal female preferred the male with thehigher courtship rate; whereas when the receptive female spawned,the focal female preferred the spawning male. Our results suggestthat female medaka prefer actively courting males, unless theyhave the opportunity to copy the mate choice of another female.     

Male Reproductive Success in a Promiscuous Armoured Catfish Corydoras Aeneus (Callichthyidae)

Among a variety of fish mating systems, promiscuity with random-mating seems to be most prevalent. However, detailed studies of promiscuity have been rare due partly to the peculiar difficulty in examination of male mating and reproductive success in the random mating. Females of the armoured catfish Corydoras aeneus (no sexual dimorphism other than size of males > females) spawn 10–20 egg-clutches with multiple males at a time, but an entire egg clutch is inseminated by sperm of a single male. We studied mating system of this fish in aquarium. Males had neither mating territories nor monopolized females, never being aggressive against rival males. Evidence of female preference for certain male traits including size was not detected. Females mated a male in proportion to his relative courtship frequency among males. Courtship frequency was not related to male size, and male mating success was not different between small and large males. Clutch size and insemination rate were different neither between small and large males nor between frequently and less frequently courting males. Thus, the male reproductive success will not be related to the male size, but directly to courtship frequency, indicating the random mating in this fish. There seemed to be fecundity advantage with size in female, and the consequent sexual difference in energy allocation will be responsible to the sexual dimorphism. We also discuss the low male-GSI in this promiscuous fish in which sperm competition hardly occurred.     

Size‐Dependent Male Mate Preference and its Association with Size‐Assortative Mating in a Mangrove Snail,Littoraria ardouiniana

In many animals, body size plays a crucial role in mating success in the context of competition and preference for mates. Increasing evidence has shown that male mate preference can be size‐dependent and, therefore, an important driver of size‐assortative mating. To test this theory, mate choice experiments were performed during the three consecutive stages of mating behaviour, namely trail following, shell mounting and copulation, in the dioecious mangrove snail, Littoraria ardouiniana. These experiments identified two possible forms of size‐dependent male mate preference which could contribute to the formation of size‐assortative mating in these snails. Firstly, whereas small males were unselective, large males were selective and preferred to follow mucus trails laid by large females. Alternatively, the results can also be interpreted as all males were selective and adopted a mating strategy of selecting females similar to, or larger than, their own sizes. Both small and large males also copulated for longer with large than with small females, and this was more pronounced in large males. When two males encountered a female, they engaged in physical aggression, with the larger male excluding the smaller male from copulating with the female. This study, therefore, demonstrated that size‐dependent male mate preference may, along with male–male competition, play an important role in driving size‐assortative mating in these mangrove snails, and this may also be the case in other species that exhibit male mate choice.     

Preference polymorphism for coloration but no speciation in a population of Lake Victoria cichlids

Female mating preference based on male nuptial coloration hasbeen suggested to be an important source of diversifying selectionin the radiation of Lake Victoria cichlid fish. Initial variationin female preference is a prerequisite for diversifying selection;however, it is rarely studied in natural populations. In clearwater areas of Lake Victoria, the sibling species Pundamiliapundamilia with blue males and Pundamilia nyererei with redmales coexist, intermediate phenotypes are rare, and most femaleshave species-assortative mating preferences. Here, we studya population of Pundamilia that inhabits turbid water wheremale coloration is variable from reddish to blue with most malesintermediate. We investigated male phenotype distribution andfemale mating preferences. Male phenotype was unimodally distributedwith a mode on intermediate color in 1 year and more blue-shiftedin 2 other years. In mate choice experiments with females ofthe turbid water population and males from a clearer water population,we found females with a significant and consistent preferencefor P. pundamilia (blue) males, females with such preferencesfor P. nyererei (red) males, and many females without a preference.Hence, female mating preferences in this population could causedisruptive selection on male coloration that is probably constrainedby the low signal transduction of the turbid water environment.We suggest that if environmental signal transduction was improvedand the preference/color polymorphism was stabilized by negativefrequency-dependent selection, divergent sexual selection mightseparate the 2 morphs into reproductively isolated species resemblingthe clear water species P. pundamilia and P. nyererei.     

Do male two-spotted gobies prefer large fecund females?

A male mating preference for large females may be expected whenfemale size is correlated with fecundity. We tested for sucha preference in a fish, the two-spotted goby (Gobiusculus flavescens,Gobiidae), for which a male preference for colorful femaleshas been demonstrated. We offered males a choice between twostimulus females of different size, controlling for female colorand stage of egg maturation. We also analyzed the relationshipbetween size and fecundity (total number of eggs in the clutch)by allowing females of different size to spawn in a controlledenvironment. Female length explained 37% of the variation infecundity, but males showed only a weak preference for largefemales. We compared the coefficient of variation (CV) in fecunditybetween female two-spotted gobies and other fish species forwhich male preferences for large females have been reported.The CV in fecundity in the two-spotted goby was among the lowest.We suggest that the low variation limits the potential fecunditybenefit to be gained by a male selecting females on the basisof size alone. Our study emphasizes the importance of the variationin partner quality for the direction and the strength of matepreferences, as suggested by theoretical models.     

Pre‐ and postcopulatory sexual selection act in concert to determine male reproductive success in Tribolium castaneum

To capture how sexual selection shapes male reproductive success across different stages of reproduction in Tribolium castaneum (Coleoptera, Tenebrionidae), we combined sequential sperm defence (P1) and sperm offence (P2) trials with additional trials where both males were added simultaneously to the female. We found a positive correlation between the relative paternity share in simultaneous male–male competition trials and the P2 trial. This suggests that males preferred by females as sires achieve superior fertilization success during sperm competition in the second male position. In simultaneous male–male competition trials, where pre‐, peri‐ and postcopulatory sexual selection were all allowed to act, the relative paternity share of preferred males was more than 20% higher than in P2 sperm competition trials where precopulatory female choice was disabled. Additional behavioural observations revealed that mating with more attractive males resulted significantly more frequently in offspring production than mating with less attractive males. Thus, by comparing male fertilization success in trials where precopulatory choice was turned off with more inclusive estimates of fertilization success where pre‐ and pericopulatory choice could occur, we show that female mate choice may effectively inhibit sperm competition. Female mate choice and sperm competition (P2) are positively correlated, which is consistent with directional sexual selection in this species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 67–75.     

Repeatability of mate choice in female red jungle fowl

We staged female mate choice trials between pairs of males andrepeated the process for each female to determine the repeatabilityof female preference for males in red jungle fowl (Gallus gallus)in the first and second half of the breeding season. We measuredmale morphological traits (the size and color of the comb andthe brightness of the hackle feathers) that females are knownto use in choosing a mate. In the first half of the breedingseason, females showed repeatability in their choices of matewith respect to the male's comb characters. Females did notshow a repeatable preference with respect to male hackle feathers,and we found no repeatability of mate choice in the second halfof the season. Females seem to primarily look at the male'scomb when choosing a mate, and other ornaments seem only ofsecondary importance.[Behav Ecol 7: 243-246 (1996)]     

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.     

Do Female Mandrills Prefer Brightly Colored Males?

Although secondary sexual adornments are widespread in male primates, few studies have examined female choice for these characters. Mandrills (Mandrillus sphinx) present an extreme example of sexual dimorphism, with males exhibiting an array of striking adornments. The most dominant adult male in a group exhibits the brightest and most extensive red coloration, while the other males are less brightly colored. I examined whether female mandrills prefer brightly colored males using data on periovulatory sexual behavior during the 1996 mating season for all males 8 years old (n = 5) and all parous females (n = 9) in a semifree-ranging colony at CIRMF, Gabon. Brightness of male coloration is significantly positively correlated with time spent within 2 m of females, female responsibility for proximity, number of sexual presentations received, % approaches accepted by females, and % inspections with which females cooperated. Females also groomed only the brightest male. Behaviors indicating female preference are not correlated significantly with male dominance rank, and partial correlations confirm that the influence of male color on female behavior is stronger than that of male rank. With the influence of male dominance rank controlled, correlation coefficients between female behaviors and male mating success are high and positive. In further support of the hypothesis that females show mate choice for brightly colored males, independent of dominance rank, I report an unusual case wherein the alpha male fell in rank without loss of coloration. He experienced no significant change in female responsibility for proximity, sexual presentations received, or female reaction to approaches or inspections, though he was no longer observed to mate. Accordingly, female mandrills attend to differences in male secondary sexual characters and favor brightly colored males. As brightly colored males are also dominant this reinforces the influence of male-male competition on male reproductive success and may explain the very high reproductive skew in mandrill males and their extraordinary appearance.     

Nonrandom pairing by male barn owls (Tyto alba) with respect to a female plumage trait

In socially monogamous species it is rare for females to bemore intensely colored than males. The barn owl (Tyto alba)is one of the exceptions, as females usually exhibit more andlarger black spots on the plumage. The evolution of sexual dimorphismin plumage traits is commonly assumed to be the result of sexualselection. I therefore examined the prediction that male barnowls do not pair randomly with respect to female plumage spottinessduring a 5-year study in Switzerland. The prediction was supported,as males that changed mates acquired a new female that was similarlyspotted to the previous one, and pairing with respect to plumage spottinesswas positively assortative. Significant repeatability in male pairingwas presumably neither the consequence of sharing the same habitats withfemales displaying a given plumage spottiness nor of morphological characteristicsof the males that could influence mate sampling. A resemblance inplumage spottiness between the mates of sons and of their fathersuggests that repeatability could have resulted from sexualimprinting and/or heritable variance in male preference forspotted females. To test whether males assess female plumagespottiness, I either cut off black spots or small pieces of feathersbut not the spots of already mated females. Males mated to females withreduced plumage spottiness fed their brood at a lower cadencyand achieved a lower reproductive success than other males.This experiment further suggests that female plumage spottinessis a stimulus for males.     

Male body length influences mate-choice copying in the sailfin molly Poecilia latipinna

Females can choose a male independently of other females' matepreferences, or they can copy the mate choice of other females.Alternatively, mate-choice copying and independent mate choicecan interact if females assess male traits when deciding whetheror not to copy. We investigated how mate-choice copying interactswith a preference for large males in the sailfin molly (Potecilialatipinna). Sailfin molly females exhibited a preference forlarger males. They also copied the mate choice of other femaleswhen males were of similar body length. Females did not copy,however, when males differed substantially in body length. Ourresults show that conspecific mate copying occurs in the sailfinmolly but does not override a preference for larger males.     

Sequential mate encounters: female but not male body size influences female remating behavior

Whether and how individuals choose sequentially among matesis an important but largely neglected aspect in sexual selectionstudies. Here, we explore female remating behavior in the cellarspider Pholcus phalangioides. We focus on body size as one ofthe most important traits involved in mate choice. Large andsmall females (n = 216) were double mated with large or smallmales in all eight possible combinations. All females copulatedwhen virgin, but only 82% accepted a second male. The chanceof a female remating was not significantly predicted by thebody size of the second or first male or by the size differencebetween the two. In contrast, a previous study demonstrateda male size effect in that larger males monopolized femalesuntil egg laying when two males of different sizes were present.We suggest that sequential encounters are more common undernatural conditions than male monopolization of females becauseestimates of concurrent multiple paternity together with observationsin a natural population do not favor mate guarding as the predominantmating strategy in this species. It follows from our study thatthe intensity of sexual selection on male size may be greatlyoverestimated when using a competitive laboratory setting fora species in which females generally encounter mates in a sequentialfashion. Female remating probability was significantly predictedby female size, with large females remating with higher probabilitythan small females. Thus, when mating with large females, malesmay gain higher fertilization success through increased femalefecundity but also face a higher sperm competition risk.