Experimental evolution of a sexually selected display in yeast

The fundamental principle underlying sexual selection theory is that an allele conferring an advantage in the competition for mates will spread through a population. Remarkably, this has never been demonstrated empirically. We have developed an experimental system using yeast for testing genetic models of sexual selection. Yeast signal to potential partners by producing an attractive pheromone; stronger signallers are preferred as mates. We tested the effect of high and low levels of sexual selection on the evolution of a gene determining the strength of this signal. Under high sexual selection, an allele encoding a stronger signal was able to invade a population of weak signallers, and we observed a corresponding increase in the amount of pheromone produced. By contrast, the strong signalling allele failed to invade under low sexual selection. Our results demonstrate, for the first time, the spread of a sexually selected allele through a population, confirming the central assumption of sexual selection theory. Our yeast system is a powerful tool for investigating the genetics of sexual selection.     

I'm sexy and I glow it: female ornamentation in a nocturnal capital breeder

In many species, males rely on sexual ornaments to attract females. Females, by contrast, rarely produce ornaments. The glow-worm (Lampyris noctiluca) is an exception where wingless females glow to attract males that fly in search of females. However, little is known about the factors that promote the evolution of female ornaments in a sexual selection context. Here, we investigated if the female ornament of the glow-worm is a signal of fecundity used in male mate choice. In support of this, we found brightness to correlate with female fecundity, and males to prefer brighter dummy females. Thus, the glow emitted by females is a reliable sexual signal of female fecundity. It is likely that male preference for the fecundity-indicating ornament has evolved because of large variation among females in fecundity, and because nocturnal males cannot directly assess female size and fecundity. These results indicate that female ornamentation may evolve in capital breeders (i.e. those in which stored resources are invested in reproduction) when females vary significantly in fecundity and this variation cannot be assessed directly by males.     

Exposure to sexual signals during rearing increases immune defence in adult field crickets

Increased investment in immunity is expected to be beneficial under crowded conditions because of the greater risk of pathogen and parasite transmission, but the evolution of this facultative response relies on the ability to accurately assess social cues in the environment and adjust immune defences accordingly. Because of their highly conspicuous nature, long-range sexual signals are prime candidates to be used in evaluating the social conditions likely to be experienced upon adulthood in continuously breeding species; however, their role in mediating immune responses is unknown. We tested whether exposure to acoustic sexual signals in the field cricket Teleogryllus oceanicus affects immunity by manipulating male juvenile experience of acoustic signals, and measuring the effect on adult immunity. Adult males exposed to song during rearing showed stronger immune responses than males reared in silence: they were better able to encapsulate artificial nylon implants and showed higher levels of antimicrobial lysozyme-like activity in their haemolymph. Experience of sexual signals thus translates into increased immunity, which suggests that such signals may play a role in conveying information about population demography and shaping density-dependent responses in unintended receivers.     

Do females preferentially associate with males given a better start in life?

A poor start in life owing to a restricted diet can have readily detectable detrimental consequences for many adult life-history traits. However, some costs such as smaller adult body size are potentially eliminated when individuals modify their development. For example, male mosquitofish (Gambusia holbrooki) that have reduced early food intake undergo compensatory growth and delay maturation so that they eventually mature at the same size as males that develop normally. But do subtle effects of a poor start persist? Specifically, does a male''s developmental history affect his subsequent attractiveness to females? Females prefer to associate with larger males but, controlling for body length, we show that females spent less time in association with males that underwent compensatory growth than with males that developed normally.     

Female butterflies prefer males bearing bright iridescent ornamentation

Butterflies are among nature's most colorful animals, and provide a living showcase for how extremely bright, chromatic and iridescent coloration can be generated by complex optical mechanisms. The gross characteristics of male butterfly colour patterns are understood to function for species and/or sex recognition, but it is not known whether female mate choice promotes visual exaggeration of this coloration. Here I show that females of the sexually dichromatic species Hypolimnas bolina prefer conspecific males that possess bright iridescent blue/ultraviolet dorsal ornamentation. In separate field and enclosure experiments, using both dramatic and graded wing colour manipulations, I demonstrate that a moderate qualitative reduction in signal brightness and chromaticity has the same consequences as removing the signal entirely. These findings validate a long-held hypothesis, and argue for the importance of intra- versus interspecific selection as the driving force behind the exaggeration of bright, iridescent butterfly colour patterns.     

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.     

Swingin' in the rain: condition dependence and sexual selection in a capricious world

Signals used in mate attraction are predicted to be highly condition dependent, and thus should be sensitive to environmental contributions to condition. However, the effects of temporal fluctuations in the environment on sexual selection in long-lived animals have been largely ignored. Female superb fairy-wrens, Malurus cyaneus, use the time that males moult into nuptial plumage prior to the onset of the breeding season to distinguish between the extra-group sires that dominate paternity. Although moult varies predictably with age, and shows marked differences between males, the phenotypic distribution also changes radically with climate; so after dry summers few males can attempt early moult. We use the recently introduced de-lifing technique to examine sexual selection gradients over 15 years of selection. Overall, there was strong evidence of directional sexual selection for early moult. However, sexual selection was much stronger when the conditions were favourable (rainfall was high), and selection was undetectable in some years. The contribution of early moulting males to population growth increased when many males moulted early, decreased when early moulting males suffered disproportionate mortality and decreased when females lacked subordinate helpers, forcing them to cede paternity to their social partner. These data suggest that short-term and laboratory studies of mate choice and sexual selection may misrepresent or underestimate the complexity of the sexual selection landscape.     

Male-derived cuticular hydrocarbons signal sperm competition intensity and affect ejaculate expenditure in crickets

Female sexual promiscuity can have significant effects on male mating decisions because it increases the intensity of competition between ejaculates for fertilization. Because sperm production is costly, males that can detect multiple matings by females and allocate sperm strategically will have an obvious fitness advantage. The presence of rival males is widely recognized as a cue used by males to assess sperm competition. However, for species in which males neither congregate around nor guard females, other more cryptic cues might be involved. Here, we demonstrate unprecedented levels of sperm competition assessment by males, which is mediated via the use of chemical cues. Using the cricket Teleogryllus oceanicus, we manipulated male perception of sperm competition by experimentally coating live unmated females with cuticular compounds extracted from males. We found that males adjusted their ejaculate allocation in response to these compounds: the viability of sperm contained within a male's ejaculate decreased as the number of male extracts applied to his virgin female partner was increased. We further show that males do not respond to the relative concentration of male compounds present on females, but rather to the number of distinct signature odours of individual males. Our results conform to sperm competition theory, and show for the first time, to our knowledge, that males can detect different intensities of sperm competition by using distinct chemical cues of individual males present on females.     

Females prefer to associate with males with longer intromittent organs in mosquitofish

Sexual selection is a major force behind the rapid evolution of male genital morphology among species. Most within-species studies have focused on sexual selection on male genital traits owing to events during or after copulation that increase a male''s share of paternity. Very little attention has been given to whether genitalia are visual signals that cause males to vary in their attractiveness to females and are therefore under pre-copulatory sexual selection. Here we show that, on average, female eastern mosquitofish Gambusia holbrooki spent more time in association with males who received only a slight reduction in the length of the intromittent organ (‘gonopodium’) than males that received a greater reduction. This preference was, however, only expressed when females chose between two large males; for small males, there was no effect of genital size on female association time.     

Male fish use prior knowledge about rivals to adjust their mate choice

Mate choice as one element of sexual selection can be sensitive to public information from neighbouring individuals. Here, we demonstrate that males of the livebearing fish Poecilia mexicana gather complex social information when given a chance to familiarize themselves with rivals prior to mate choice. Focal males ceased to show mating preferences when being observed by a rival (which prevents rivals from copying mating decisions), but this effect was only seen when focal males have perceived rivals as sexually active. In addition, focal males that were observed by a familiar, sexually active rival showed a stronger behavioural response when rivals were larger and thus, more attractive to females. Our study illustrates an unparalleled adjustment in the expression of mating preferences based on social cues, and suggests that male fish are able to remember and strategically exploit information about rivals when performing mate choice.     

Beyond species recognition: somatic state affects long-distance sex pheromone communication

Long-range sex pheromones have been subjected to substantial research with a particular focus on their biosynthesis, peripheral perception, central processing and the resulting orientation behaviour of perceivers. Fundamental to the research on sex attractants was the assumption that they primarily coordinate species recognition. However, especially when they are produced by the less limiting sex (usually males), the evolution of heightened condition dependence might be expected and long-range sex pheromones might, therefore, also inform about a signaller''s quality. Here we provide, to our knowledge, the first comprehensive study of the role of a male''s long-range pheromone in mate choice that combines chemical analyses, video observations and field experiments with a multifactorial manipulation of males'' condition. We show that the emission of the long-distance sex pheromone of the burying beetle, Nicrophorus vespilloides is highly condition-dependent and reliably reflects nutritional state, age, body size and parasite load—key components of an individual''s somatic state. Both, the quantity and ratio of the pheromone components were affected but the time invested in pheromone emission was largely unaffected by a male''s condition. Moreover, the variation in pheromone emission caused by the variation in condition had a strong effect on the attractiveness of males in the field, with males in better nutritional condition, of older age, larger body size and bearing less parasites being more attractive. That a single pheromone is influenced by so many aspects of the somatic state and causes such variation in a male''s attractiveness under field conditions was hitherto unknown and highlights the need to integrate indicator models of sexual selection into pheromone research.     

Encoding choosiness: female attraction requires prior physical contact with individual male scents in mice

Scents, detected through both the main and vomeronasal olfactory systems, play a crucial role in regulating reproductive behaviour in many mammals. In laboratory mice, female preference for airborne urinary scents from males (detected through the main olfactory system) is learnt through association with scents detected through the vomeronasal system during contact with the scent source. This may reflect a more complex assessment of individual males than that implied by laboratory mouse studies in which individual variation has largely been eliminated. To test this, we assessed female preference between male and female urine using wild house mice with natural individual genetic variation in urinary identity signals. We confirm that females exhibit a general preference for male over female urine when able to contact urine scents. However, they are only attracted to airborne urinary volatiles from individual males whose urine they have previously contacted. Even females with a natural exposure to many individuals of both sexes fail to develop generalized attraction to airborne male scents. This implies that information gained through contact with a specific male's scent is essential to stimulate attraction, providing a new perspective on the cues and olfactory pathways involved in sex recognition and mate assessment in rodents.