Sex-role reversal revisited: choosy females and ornamented, competitive males in a pipefish

In the pipefish Syngnathus typhle sex roles are reversed, thatis, females compete more intensely than males over mates. However,competition over mates among individuals of one sex does notnecessarily prevent members of that same sex from being choosy,and choosiness in the other sex does not prevent competitionwithin it. In an experiment we allowed a female pipefish tochoose freely between two males, after which we released themales and let the three interact. Comparisons with earlier resultsshow that both sexes courted partners and competed with consexuals.However, females courted more often than did males, and courtshipwas more frequent in treatments involving large individualsthan in treatments with small individuals. Males competed amongthemselves for access to mates but for a shorter duration thanfemales in the same situation. Males displayed an ornament towardsfemales but not to males during mating competition. Females,however, used their ornament in both contexts. Females did notalways mate with the male of their previously made choice, whichwe interpret as females being constrained by male-male competition,male motivation to mate, or both. Thus, in this sex-role reversedspecies, mate choice in the more competitive sex may be circumventedand even overruled by mate competition and mating willingnessin the least competitive sex. Hence, sex roles should not beconsidered as sexes being either choosy or competitive but ratherthat males and females may exhibit different combinations ofchoice and competition.     

An intimidating ornament in a female pipefish

A sexually selected signal may serve a dual function being bothattractive to mates and deterring rivals. Presently, there arefew unambiguous demonstrations of an ornament functioning inboth a mate choice and mate competition context and none regardingfemale ornaments. We have shown earlier that a temporary ornament,a striped pattern, in a sex-role reversed female pipefish, Syngnathustyphle, attracts males. Here we show that this ornament alsointimidates rival females: in one experiment a male could interactwith either 1 or 2 females. Latency until copulation was longerwhen 2, rather than 1, females were present. Moreover, when2 females were present, competition lasted longer and time untilmating took place increased when females displayed their ornamentsmore equally. In another experiment, a focal female could see1 stimulus female and 1 stimulus male, the latter 2 being unawareof each other. The ornament of the stimulus female was manipulated,either strengthened by being painted black or left unalteredby being sham-painted. As a result, focal females experiencingblack-painted stimulus females decreased courtship as well ascompetitive activities compared with focal females seeing sham-paintedfemales. Moreover, focal females seeing black-painted femalesdisplayed less of their own ornament compared with controls.This decrease was due to a decrease in display toward malesrather than to stimulus females. Thus, this female ornamentindeed has a dual function, attracting mates and deterring rivals.In addition, the social costs invoked by this intimidating effecton rivals may help to maintain signal honesty.     

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.     

Parasites make male pipefish careless

Parasite-mediated sexual selection is expected to favour the avoidance of matings with infected individuals. However, the extent to which the costs and benefits of discriminating against parasitized mates trade off may depend upon numerous factors. I investigated the effects of sex and infection status on choosiness in sex-role reversed deep-snouted pipefish (Syngnathus typhle L.) that were either artificially infected with the trematode parasite Cryptocotyle sp. or sham-infected. Sham-infected males were significantly more likely to associate with a sham-infected female rather than with a Cryptocotyle-infected female. Infected males failed to discriminate against infected potential partners. Males were choosier the larger they were relative to the females available for choice. Females were not discriminatory, regardless of their infection status. Given an inverse relation between female fecundity and parasite load, choosy unparasitized males may gain enhanced reproductive success from their choice decisions. In contrast, more heavily infected wild-caught males gave birth to slightly fewer, but not smaller offspring than did uninfected or lightly infected males, suggesting only a low direct premium on choosy females. The detrimental effects of parasitism on male choosiness, and the lack of female discrimination against infected males likely have profound repercussions on the strength of sexual selection acting on the two sexes and on the dynamics of host-parasite interactions in this system.     

Genes, copying, and female mate choice: shifting thresholds

Recent experimental work on guppies (Poecilia reticulata) hasexamined the strength of genetic and cultural (copying) factorsin determining female mate choice. Using females from a populationwith a heritable preference for the amount of orange body colorpossessed by males, prior work discovered that a threshold differencein orange color among males existed below which females wouldchoose a less orange male if they observed another female choosethat male, but above which they consistently preferred the moreorange of the males, regardless of whether they viewed anotherfemale prefer the less orange male. I tested whether this thresholdcan be shifted by increasing the amount of mate-copying informationavailable to a female. I demonstrate that when a female hasthe opportunity to see two different model females independentlyprefer the less orange of two males or a single female neara drab male for a longer period of time (twice as long as inprior work), the observer female prefers this drab male evenwhen males dramatically differ in orange coloration.     

Fewer newborn result in superior juveniles in the paternally brooding pipefish Syngnathus typhle L.

In the pipefish Syngnathus typhle L. parental care is exclusively paternal. Males brood embryos in a brood pouch for about a month, providing nutrients and oxygen. The newborn juveniles are free-swimming and no further care is provided. The influence of paternal length and number of newborn on juvenile weight and growth rate, and how in turn the latter relates to juvenile survival, were investigated. It was found, using partial correlations, that paternal length is significantly and positively correlated to weight of newborn, weight of a two-week-old juvenile and juvenile growth rate (weight increment day^-1). Furthermore, number of newborn is correlated negatively to weight of newborn, weight after two weeks and juvenile growth rate. In an experiment in which juvenile pipefish of different sizes were exposed to predation it was shown that larger juveniles survived better. It is concluded that, in S. typhle , large juvenile size and rapid juvenile growth positively influence offspring performance. Offspring performance is positively influenced by paternal length which, however, may be a consequence of larger males receiving larger eggs. The number of newborn, i.e. the number of siblings in the male's pouch, has a negative effect on offspring performance, independently of other factors. Thus, the results show that for males the benefits of having superior juveniles will be at the cost of having fewer offspring.     

Male mate choice relies on major histocompatibility complex class I in a sex‐role‐reversed pipefish

Mate choice for compatible genes is often based on genes of the major histocompatibility complex (MHC). Although MHC‐based mate choice is commonly observed in female choice, male mate choice remains elusive. In particular, if males have intense paternal care and are thus the choosing sex, male choice for females with dissimilar MHC can be expected. Here, we investigated whether male mate choice relies on MHC class I genes in the sex‐role reversed pipefish Syngnathus typhle. In a mate choice experiment, we determined the relative importance of visual and olfactory cues by manipulating visibility and olfaction. We found that pipefish males chose females that maximize sequence‐based amino acid distance between MHC class I genotypes in the offspring when olfactory cues were present. Under visual cues, large females were chosen, but in the absence of visual cues, the choice pattern was reversed. The use of sex‐role reversed species thus revealed that sexual selection can lead to the evolution of male mate choice for MHC class I genes.     

Temperature affects male and female potential reproductive rates differently in the sex-role reversed pipefish, Syngnathus typhle

The differences in potential reproductive rate between the sexescan be used to predict the operational sex ratio and the patternsand intensity of mating competition and hence sexual selectionin a population. This article describes how one environmentalcomponent, temperature, affects potential reproductive ratesof the two sexes in the paternally brooding, sex-role reversedpipefish (Syngnathus typhle). Males brooded embryos much longer(on average 58 days) in cold water (about 10°C) than inwarmer water (35 days at about 15°C). As a consequence,the potential reproductive rate (number of eggs brooded perday) of males was significantly higher in warm water. In females,however, potential reproductive rate, i.e., number of eggs producedper day given an unlimited access to mates, was not significantlydifferent between temperatures. In both sexes, potential reproductiverate was positively related to body size. At both temperatures,females had the potential to reproduce faster than males. Asa result, the operational sex ratio will become female biasedand sex-roles reversed, as is the case in this species. Sincetemperature differently influenced the potential reproductiverates of males and females, with the sexual difference largerat lower temperatures, more intense female-female competitionis predicted at low temperatures.     

No terminal investment in pipefish males: only young males exhibit risk-prone courtship behavior

Animals are expected to trade-off current and future reproductionin order to maximize lifetime reproductive success. Old individualsmay accept higher risks during courtship and mate choice astheir residual reproductive value (RRV) diminishes (the terminalinvestment hypothesis). Alternatively, young individuals maybe forced to take higher risks during courtship to compensatefor their lower competitiveness and/or attractiveness (the compensationhypothesis). In this study, we used the sex-role reversed pipefishSyngnathus typhle to test how mate choice and courtship behaviorof males with different RRV were affected by an increase inpredation risk. Males of different ages were given the opportunityto court and choose between 2 partners. In half of the trials,a predator was present in a separate aquarium. We found no supportfor the terminal investment hypothesis: no difference in responseto the increased predation risk by males of different ages wasevident. In agreement with the compensation hypothesis, youngmales invested more in courtship behavior compared with oldermales. In addition, in the absence of a predator, we found thata high female activity was important for male mate choice decisions.During increased predation risk, this relationship was, however,reversed and males preferred less active, and thus less conspicuous,partners. This suggests that both female activity and size areimportant factors for male mating decisions in this speciesand that these decisions mainly are affected by predation riskand advantages in mate acquisition.     

Nonindependent mating in a coral reef damselfish: evidence of mate choice copying in the wild

Theoretical and experimental studies have shown that mate choicecopying is a viable mating strategy under certain conditions.Copying experiments in fish have been conducted primarily inthe laboratory, except for one study conducted in the fieldunder artificial conditions. We investigated whether in a wildpopulation of the coral reef whitebelly damselfish (Amblyglyphidodonleucogaster) females copy the choice of other females. Femalespreferentially spawn with males that have recently mated. Todetermine if the presence of new eggs in the nest was the reasonfemales chose mates or whether females were mate choice copying,we conducted egg-switching experiments. Eggs from males thatrecently mated were donated to males that had no eggs. If femalesare mate choice copying, then donor males with no eggs in thenest should continue to receive additional eggs. If femalesare using the presence of new eggs as the criterion for matechoice, then foster males with new eggs should receive additionaleggs. We found that donor males received new eggs significantlymore often than expected. More females mated with donor malesthan foster males. Furthermore, females preferentially choseto mate with males whom they had seen mating with another female.Females appear to remember the mate choice of other femalesand choose to mate with those same males even after 1 day. Theseresults suggest that females may be copying the mating decisionof other females rather than choosing males based on the presenceof new eggs in the nest.     

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.     

Human mate choice and the wedding ring effect

Individuals are often restricted to indirect cues when assessing the mate value of a potential partner. Females of some species have been shown to copy each other’s choice; in other words, the probability of a female choosing a particular male increases if he has already been chosen by other females. Recently it has been suggested that mate-choice copying could be an important aspect of human mate choice as well. We tested one of the hypotheses, the so-called wedding ring effect—that women would prefer men who are already engaged or married—in a series of live interactions between men and women. The results show that women do not find men signaling engagement, or being perceived as having a partner, more attractive or higher in socioeconomic status. Furthermore, signs of engagement did not influence the women’s reported willingness to engage in short-term or long-term relationships with the men. Thus, this study casts doubt on some simplified theories of human mate-choice copying, and alternative, more complex scenarios are outlined and discussed. Tobias Uller works on broad issues in evolutionary biology, such as life-history evolution and evolutionary genetics. Christoffer Johansson recently received his Ph.D. with a dissertation on biomechanics of swimming birds. Their collaborative work on humans is focused on mate choice.     

The operational sex ratio influences choosiness in a pipefish

If more females than males are available for mating in the breedingpopulation (i.e., the operational sex ratio, OSR, is femalebiased), males can afford to be choosy. In the pipefish (Syngnathustyphle) females compete for males, who are choosy. In natureOSRs are typically female biased, but may occasionally be malebiased. In a series of experiments, males were allowed to choosebetween a large and a small female under a perceived excessof either males or females. Under female bias, males preferredthe large female: they spent more time close to her than tothe small female; they courted the large female sooner thanthe small; and they tended to copulate sooner and more oftenwith the large female. Under male bias all these differencesvanished and males mated at random with respect to female size.Males reproduced at a faster rate under male than under femalebias because they received more eggs in their brood pouches.Thus, males switched from maximizing mate quality (i.e., beingchoosy) to minimizing the risk of not reproducing (i.e., beingquick) as the OSR became male biased.     

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)]     

Male Sailfin mollies (Poecilia latipinna) copy the mate choice of other males

Female mate-copying has been shown to occur between heterospecifics:female sailfin mollies Poecilia latipinna copy the choice oftheir gynogenetic associates, Amazon mollies P. formosa. Femalemate-copying thus contributes to the maintenance of this asexual-sexualspecies complex by providing an advantage to male sailfin molliesthat mate with Amazon females; because of mate-copying thesemales increase their attractiveness to conspecific females.Here we show that male mate-copying, an unreported phenomenon,also occurs and that it can reverse male preferences for conspecificfemales. Male mate-copying should also contribute to the maintenanceof gynogens and might be advantageous in allowing males a meansto rapidly assess female receptivity although sometimes resultingin heterospedfic matings.     

The evolution of male mate choice in insects: a synthesis of ideas and evidence

Mate choice by males has been recognized at least since Darwin's time, but its phylogenetic distribution and effect on the evolution of female phenotypes remain poorly known. Moreover, the relative importance of factors thought to underlie the evolution of male mate choice (especially parental investment and mate quality variance) is still unresolved. Here I synthesize the empirical evidence and theory pertaining to the evolution of male mate choice and sex role reversal in insects, and examine the potential for male mating preferences to generate sexual selection on female phenotypes. Although male mate choice has received relatively little empirical study, the available evidence suggests that it is widespread among insects (and other animals). In addition to 'precopulatory' male mate choice, some insects exhibit 'cryptic' male mate choice, varying the amount of resources allocated to mating on the basis of female mate quality. As predicted by theory, the most commonly observed male mating preferences are those that tend to maximize a male's expected fertilization success from each mating. Such preferences tend to favour female phenotypes associated with high fecundity or reduced sperm competition intensity. Among insect species there is wide variation in mechanisms used by males to assess female mate quality, some of which (e.g. probing, antennating or repeatedly mounting the female) may be difficult to distinguish from copulatory courtship. According to theory, selection for male choosiness is an increasing function of mate quality variance and those reproductive costs that reduce, with each mating, the number of subsequent matings that a male can perform ('mating investment') Conversely, choosiness is constrained by the costs of mate search and assessment, in combination with the accuracy of assessment of potential mates and of the distribution of mate qualities. Stronger selection for male choosiness may also be expected in systems where female fitness increases with each copulation than in systems where female fitness peaks at a small number of matings. This theoretical framework is consistent with most of the empirical evidence. Furthermore, a variety of observed male mating preferences have the potential to exert sexual selection on female phenotypes. However, because male insects typically choose females based on phenotypic indicators of fecundity such as body size, and these are usually amenable to direct visual or tactile assessment, male mate choice often tends to reinforce stronger vectors of fecundity or viability selection, and seldom results in the evolution of female display traits. Research on orthopterans has shown that complete sex role reversal (i.e. males choosy, females competitive) can occur when male parental investment limits female fecundity and reduces the potential rate of reproduction of males sufficiently to produce a female-biased operational sex ratio. By contrast, many systems exhibiting partial sex role reversal (i.e. males choosy and competitive) are not associated with elevated levels of male parental investment, reduced male reproductive rates, or reduced male bias in the operational sex ratio. Instead, large female mate quality variance resulting from factors such as strong last-male sperm precedence or large variance in female fecundity may select for both male choosiness and competitiveness in such systems. Thus, partial and complete sex role reversal do not merely represent different points along a continuum of increasing male parental investment, but may evolve via different evolutionary pathways.