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.     

Adult sex ratio variation: implications for breeding system evolution

Adult sex ratio (ASR) exhibits immense variation in nature, although neither the causes nor the implications of this variation are fully understood. According to theory, the ASR is expected to influence sex roles and breeding systems, as the rarer sex in the population has more potential partners to mate with than the more common sex. Changes in mate choice, mating systems and parental care suggest that the ASR does influence breeding behaviour, although there is a need for more tests, especially experimental ones. In the context of breeding system evolution, the focus is currently on operational sex ratios (OSRs). We argue that the ASR plays a role of similar importance and urge researchers to study the ASR and the OSR side by side. Finally, we plead for a dynamic view of breeding system evolution with feedbacks between mating, parenting, OSR and ASR on both ecological and evolutionary time scales.     

Bateman's principle and immunity in a sex-role reversed pipefish

In diverse animal species, from insects to mammals, females display a more efficient immune defence than males. Bateman's principle posits that males maximize their fitness by increasing mating frequency whereas females gain fitness benefits by maximizing their lifespan. As a longer lifespan requires a more efficient immune system, these implications of Bateman's principle may explain widespread immune dimorphism among animals. Because in most extant animals, the provisioning of eggs and a higher parental investment are attributes of the female sex, sex-role reversed species provide a unique opportunity to assess whether or not immune dimorphism depends on life history and not on sex per se. In the broad-nosed pipefish Syngnathus typhle, males brood and nourish the eggs in a ventral pouch and thus invest more into reproduction than females. We found males to have a more active immune response both in field data from four populations and also in an experiment under controlled laboratory conditions. This applied to different measures of immunocompetence using innate as well as adaptive immune system traits. We further determined the specificity of immune response initiation after a fully factorial primary and secondary exposure to a common marine pathogen Vibrio spp. Males not only had a more active but also a more specific immune defence than females. Our results thus indeed suggest that the sex that invests more into the offspring has the stronger immune defence.     

Male but not female pipefish copy mate choice

If mate choice is costly, an individual may reduce the costsof choice by observing and copying the mate choice of others.Although copying has received much attention during the past10 years, evidence of copying is not very strong, partly becauseof problems with distinguishing copying from other mechanismscreating similar mating patterns. I conducted an aquarium experimentusing the deep-snouted pipefish Syngnathus typhle, a specieswith reversed sex roles and mutual mate choice. I tested whethercopying occurred both during male and female mate choice. Theresults showed that males, but not females, displayed more towardan individual, which they perceived as popular among others,and this was interpreted as male mate choice copying. Whilebeing the first evidence of copying in a sex-role–reversedspecies, the sex difference in behavior mirrors the sex-rolepattern and begs the question whether we should predict copyingonly in females in other species with mutual choice but conventionalsex roles.     

Serial monogamy and sex ratio bias in Nazca boobies

Biased operational sex ratios (OSRs) can drive sexual selection on members of the over-represented sex via competition for mates, causing higher variance and skew in reproductive success (RS) among them if an individual's quality is a persistent characteristic. Alternatively, costs of reproduction may degrade breeding performance, creating the opportunity for members of the limiting sex to switch mates adaptively, effectively homogenizing variance and skew in RS among the sex in excess. We tested these two contrasting models in a male-biased population of the Nazca booby (Sula granti) with demonstrated costs of reproduction with data on total RS over a 14-year period. Variances and skews in RS were similar, and males changed from breeder to non-breeder more frequently than females. Under the persistent individual quality model, females should mate only with high quality males, and non-breeding males should seldom enter the breeding pool, yet 45% of non-breeding males (re)entered the breeding pool each year on average. Many Nazca booby females apparently exchange a depleted male for a new mate from the pool of current non-breeder males. Our evidence linking serial monogamy to costs of reproduction is novel and suggests selection on female mating preferences based on an interaction between at least two life-history components (OSR and reproductive effort).     

Unifying cornerstones of sexual selection: operational sex ratio,Bateman gradient and the scope for competitive investment

What explains variation in the strength of sexual selection across species, populations or differences between the sexes? Here, we show that unifying two well‐known lines of thinking provides the necessary conceptual framework to account for variation in sexual selection. The Bateman gradient and the operational sex ratio (OSR) are incomplete in complementary ways: the former describes the fitness gain per mating and the latter the potential difficulty of achieving it. We combine this insight with an analysis of the scope for sexually selected traits to spread despite naturally selected costs. We explain why the OSR sometimes does not affect the strength of sexual selection. An explanation of sexual selection becomes more logical when a long ‘dry time’ (‘time out’, recovery after mating due to e.g. parental care) is understood to reduce the expected time to the next mating when in the mating pool (i.e. available to mate again). This implies weaker selection to shorten the wait. An integrative view of sexual selection combines an understanding of the origin of OSR biases with how they are reflected in the Bateman gradient, and how this can produce selection for mate acquisition traits despite naturally selected costs.     

Behavioural temperature preference in a brooding male pipefish Syngnathus typhle

In the broad‐nosed pipefish Syngnathus typhle, brooding males positioned themselves significantly more often towards the warmer part (18° C) of an aquarium, whereas females were indifferent in this respect. This behavioural temperature preference may increase male brooding rate and indirectly influence patterns of mating competition.     

Sex-role reversal of a monogamous pipefish without higher potential reproductive rate in females

In monogamous animals, males are usually the predominant competitors for mates. However, a strictly monogamous pipefish Corythoichthys haematopterus exceptionally exhibits a reversed sex role. To understand why its sex role is reversed, we measured the adult sex ratio and the potential reproductive rate (PRR), two principal factors influencing the operational sex ratio (OSR), in a natural population of southern Japan. The adult sex ratio was biased towards females throughout the breeding season, but the PRR, which increased with water temperature, did not show sexual difference. We found that an alternative index of the OSR (Sf/Sm: sex ratio of 'time in') calculated from the monthly data was consistently biased towards females. The female-biased OSR associated with sex-role reversal has been reported in some polyandrous or promiscuous pipefish, but factors biasing the OSR differed between these pipefish and C. haematopterus. We concluded that the similar PRR between the sexes in C. haematopterus does not confer reproductive benefit of polygamous mating on either sex, resulting in strict monogamous mating, and its female-biased adult sex ratio promotes female-female competition for a mate, resulting in sex-role reversal.     

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.     

Sex ratio influences the motivational salience of facial attractiveness

The sex ratio of the local population influences mating-related behaviours in many species. Recent experiments show that male-biased sex ratios increase the amount of financial resources men will invest in potential mates, suggesting that sex ratios influence allocation of mating effort in humans. To investigate this issue further, we tested for effects of cues to the sex ratio of the local population on the motivational salience of attractiveness in own-sex and opposite-sex faces. We did this using an effort-based key-press task, in which the motivational salience of facial attractiveness was assessed in samples of faces in which the ratio of male to female images was manipulated. The motivational salience of attractive opposite-sex, but not own-sex, faces was greater in the own-sex-biased (high competition for mates) than in the opposite-sex-biased (low competition for mates) condition. Moreover, this effect was not modulated by participant sex. These results present new evidence that sex ratio influences human mating-related behaviours. They also present the first evidence that the perceived sex ratio of the local population may modulate allocation of mating effort in women, as well as men.     

Behavioral responses of a sex-role reversed pipefish to a gradient of perceived predation risk

Conspicuous behaviors such as courtship and mating often makeanimals susceptible to predation. When perceiving themselvesat an elevated level of risk, animals frequently reduce conspicuousbehaviors in tradeoff for a decrease in probability of beingpreyed upon. In the present study, we used two experiments toexamine the effect of perceived predation risk from cod (Gadusmorhud) on nonreproductive and reproductive behaviors in thesex-role reversed pipefish (Syngnathus typhle). In the firstexperiment, no differences due to predation risk were detectedin the nonreproductive behaviors of either males or females.In the second experiment, predation risk had significant effectson reproductive behaviors. Pipefish were allowed to court andcopulate at four different predation levels. We created predationlevels differing in perceived predation risk by controllingthe number of sensory modes through which pipefish could detectthe presence of a cod. As predation risk increased, pipefishcopulated and courted less frequently, swam alone (displayedand searched for conspecifics) less often, and waited longerbefore commencing courtship. These changes in behavior minimizedthe amount of time spent above the eelgrass and presumably reducedconspicuousness to visual predators. Pipefish also copulatedafter a smaller amount of courtship as predation risk increased,indicating that they may trade information concerning mate qualityfor a reduction in predation risk. No differences were foundin any response variable between males and females. The roleof operational sex ratios and intersexual competition in determiningwhich sex assumes greater costs in mate acquisition is questioned.     

Size, operational sex ratio, and mate-guarding success of the carrion beetle, Necrophila americana

When male insects guard females until oviposition, the benefitsfrom last-male sperm precedence must outweigh the costs of relinquishingadditional fertilizations. The profitability of guarding isincreased when males guard large, fecund females and when femalesare scarce because fewer fertilizations are sacrificed. However,the male reproductive success is not only determined by theprofitability of guarding but also by his ability to maintainguarding. In this study, we used male carrion beetles (Necrophilaamericana) to examine the effects of sex ratio, male relativesize, and female quality on the ability to guard. First, wepresent a model of mate guarding that explores factors, suchas sperm precedence, sex ratio, male size, and female quality,that influence the profitability of postcopulatory riding. Ourmodel predicts that large N. americana males should preferentiallyguard the largest female only when the sex ratio is male biasedand sperm precedence is above 80%. In contrast, small malesgain little from guarding because they are not likely to maintainit and be the last male to mate. Then, we tested these predictionsby manipulating sex ratio, relative male size, and female quality.All males in equal sex ratio and large males in male-biasedsex ratio guarded females significantly longer than did malesin female-biased sex ratio. In male-biased sex ratio, largemales guarded significantly longer and achieved more takeoversthan small males. Large females were guarded longer. The successof guarding males in this beetle depends on their size relativeto other males and the operational sex ratio.     

Facultative adjustment of the offspring sex ratio and male attractiveness: a systematic review and meta‐analysis

Females can benefit from mate choice for male traits (e.g. sexual ornaments or body condition) that reliably signal the effect that mating will have on mean offspring fitness. These male‐derived benefits can be due to material and/or genetic effects. The latter include an increase in the attractiveness, hence likely mating success, of sons. Females can potentially enhance any sex‐biased benefits of mating with certain males by adjusting the offspring sex ratio depending on their mate's phenotype. One hypothesis is that females should produce mainly sons when mating with more attractive or higher quality males. Here we perform a meta‐analysis of the empirical literature that has accumulated to test this hypothesis. The mean effect size was small (r = 0.064–0.095; i.e. explaining <1% of variation in offspring sex ratios) but statistically significant in the predicted direction. It was, however, not robust to correction for an apparent publication bias towards significantly positive results. We also examined the strength of the relationship using different indices of male attractiveness/quality that have been invoked by researchers (ornaments, behavioural displays, female preference scores, body condition, male age, body size, and whether a male is a within‐pair or extra‐pair mate). Only ornamentation and body size significantly predicted the proportion of sons produced. We obtained similar results regardless of whether we ran a standard random‐effects meta‐analysis, or a multi‐level, Bayesian model that included a correction for phylogenetic non‐independence. A moderate proportion of the variance in effect sizes (51.6–56.2%) was due to variation that was not attributable to sampling error (i.e. sample size). Much of this non‐sampling error variance was not attributable to phylogenetic effects or high repeatability of effect sizes among species. It was approximately equally attributable to differences (occurring for unknown reasons) in effect sizes among and within studies (25.3, 22.9% of the total variance). There were no significant effects of year of publication or two aspects of study design (experimental/observational or field/laboratory) on reported effect sizes. We discuss various practical reasons and theoretical arguments as to why small effect sizes should be expected, and why there might be relatively high variation among studies. Currently, there are no species where replicated, experimental studies show that mothers adjust the offspring sex ratio in response to a generally preferred male phenotype. Ultimately, we need more experimental studies that test directly whether females produce more sons when mated to relatively more attractive males, and that provide the requisite evidence that their sons have higher mean fitness than their daughters.     

Operational sex ratio influences the opportunity for sexual selection in guppies

The opportunity for sexual selection was greater when the operational sex ratio (OSR) in guppies Poecilia reticulata was biased towards males. This could be due to an increase in both male-male competition and female mate choice under male-biased OSR.     

Within species support for the expensive tissue hypothesis: a negative association between brain size and visceral fat storage in females of the Pacific seaweed pipefish

The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the high cost of brain development and maintenance is predicted to constrain adaptive brain size evolution (the expensive tissue hypothesis, ETH). Here, we test the ETH in a teleost fish with predominant female mating competition (reversed sex roles) and male pregnancy, the pacific seaweed pipefish Syngnathus schlegeli. The relative size of the brain and other energetically expensive organs (kidney, liver, heart, gut, visceral fat, and ovary/testis) was compared among three groups: pregnant males, nonpregnant males and egg producing females. Brood size in pregnant males was unrelated to brain size or the size of any other organ, whereas positive relationships were found between ovary size, kidney size, and liver size in females. Moreover, we found that the size of energetically expensive organs (brain, heart, gut, kidney, and liver) as well as the amount of visceral fat did not differ between pregnant and nonpregnant males. However, we found marked differences in relative size of the expensive organs between sexes. Females had larger liver and kidney than males, whereas males stored more visceral fat than females. Furthermore, in females we found a negative correlation between brain size and the amount of visceral fat, whereas in males, a positive trend between brain size and both liver and heart size was found. These results suggest that, while the majority of variation in the size of various expensive organs in this species likely reflects that individuals in good condition can afford to allocate resources to several organs, the cost of the expensive brain was visible in the visceral fat content of females, possibly due to the high costs associated with female egg production.     

Natural variation in social conditions affects male mate choosiness in the amphipod Gammarus roeselii

The extent of male mate choosiness is driven by a trade-off between various environmental factors associated with the costs of mate acquisition, quality assessment and opportunity costs. Our knowledge about natural variation in male mate choosiness across different populations of the same species, however, remains limited. In this study, we compared male mate choosiness across 10 natural populations of the freshwater amphipod Gammarus roeselii (Gervais 1835), a species with overall high male mating investments, and evaluated the relative influence of population density and sex ratio (both affecting mate availability) on male mate choosiness. We investigated amplexus establishment after separating mating pairs and presenting focal males with a novel, size-matched female from the same population. Our analysis revealed considerable effects of sex ratio and (to a lesser extent) population density on time until amplexus establishment (choosiness). Male amphipods are able to perceive variable social conditions (e.g., sex ratio) and modify their mating strategy accordingly: We found choosiness to be reduced in increasingly male-biased populations, whereas selectivity increases when sex ratio becomes female biased. With this, our study expands our limited knowledge on natural variations in male mate choosiness and illustrates the importance of sex ratio (i.e., level of competition) for male mating decisions in natural environments. Accounting for variation in sex ratios, therefore, allows envisioning a distinctive variation of choosiness in natural populations and highlights the importance of considering social background information in future behavioral studies.     

The mechanism of sex ratio adjustment in a pollinating fig wasp

Sex ratio strategies in species subject to local mate competition (LMC), and in particular their fit to quantitative theoretical predictions, provide insight into constraints upon adaptation. Pollinating fig wasps are widely used in such studies because their ecology resembles theory assumptions, but the cues used by foundresses to assess potential LMC have not previously been determined. We show that Liporrhopalum tentacularis females (foundresses) use their clutch size as a cue. First, we make use of species ecology (foundresses lay multiple clutches, with second clutches smaller than first) to show that increases in sex ratio in multi-foundress figs occur only when foundresses are oviposition site limited, i.e. that there is no direct response to foundress density. Second, we introduce a novel technique to quantify foundress oviposition sequences and show, consistent with the theoretical predictions concerning clutch size-only strategies, that they produce mainly male offspring at the start of bouts, followed by mostly females interspersed by a few males. We then discuss the implications of our findings for our understanding of the limits of the ability of natural selection to produce 'perfect' organisms, and for our understanding of when different cue use patterns evolve.