Energetic cost of sexual attractiveness: ultrasonic advertisement in wax moths

Pair formation in the lesser wax moth,Achroia grisella(Lepidoptera: Pyralidae), is initiated by male ultrasonic signals that attract receptive females. Individual males vary in attractiveness to females, and the most attractive males are distinguished by exaggeration of three signal characters: pulse rate, peak amplitude and asynchrony interval (temporal separation between pulses generated by movements of the left and right wings during a given wing upstroke or downstroke). Using flow-through respirometry, we measured the resting and signalling metabolic rates of males whose relative attractiveness was known. Acoustic recordings and metabolic measurements were made simultaneously, and we calculated net metabolic rates and factorial metabolic scopes as measures for the energetic cost of signalling. On average, attractive males had higher net metabolic rates and factorial metabolic scopes than unattractive ones, but many unattractive males also had high values. Thus, high expenditure of energy on signalling is necessary but not sufficient for attractiveness. This may result because only one of the three signal characters critical for female preference, pulse rate, is correlated with energy expenditure. Although the results are consistent with the good genes model of sexual selection, they do not conflict with other indirect or direct mechanisms of female choice.     

Partitioning the Components of Sexual Selection: Attractiveness and Agonistic Behaviour in Male Wax Moths,Achroia grisella (Lepidoptera: Pyralidae)

Two components of sexual selection in the lesser wax moth, Achroia grisella, are clearly defined: females choose males based on characters of their ultrasonic advertisement signals, and males display agonistic behaviour patterns in contests over signalling stations. We conducted a series of laboratory trials to determine whether successes in these two sexual selection arenas were related. Our trials showed that winners in contests over signalling stations were characterized by earlier initiation of both signalling and aggression. These characteristics may indicate higher levels of ‘motivation,’ but it is unclear whether this level is a fixed trait. There was no relationship, however, between any measure of a male's attractiveness to females and his success in winning competition trials. Thus, inter- and intra-sexual selection may be acting on different, uncorrelated traits in A. grisella.     

When are good genes good? Variable outcomes of female choice in wax moths

Female lesser wax moths (Achroia grisella) choose males based on characters of their ultrasonic advertisement signals. Because a female''s opportunity to obtain increased somatic benefits by mating with a particular male is limited, we investigated whether females obtain genetic benefits for their offspring via mate choice. Controlled breeding experiments conducted under favourable food and temperature conditions showed that developmental characters are heritable, that sire attractiveness and offspring survivorship are unrelated, but that females mating with attractive signallers produce offspring who mature faster than the offspring of females mating with non-attractive signallers. However, under some unfavourable food or temperature conditions, it is the offspring of females mating with non-attractive males who mature faster; these offspring are heavier as well. Thus, the relationship between male attractiveness and offspring development is not environmentally robust, and support for a good genes model of mate choice in A. grisella is dependent on conditions. These findings suggest genotype–environment interactions and emphasize the necessity of testing sexual selection models under a range of natural environments.     

Genetic architecture of sensory exploitation: QTL mapping of female and male receiver traits in an acoustic moth

The evolution of extravagant sexual traits by sensory exploitation occurs if males incidentally evolve features that stimulate females owing to a pre‐existing environmental response that arose in the context of natural selection. The sensory exploitation process is thus expected to leave a specific genetic imprint, a pleiotropic control of the original environmental response and the novel sexual response in females. However, females may be subsequently selected to improve their discrimination of environmental and sexual stimuli. Accordingly, responses may have diverged and the original genetic architecture may have been modified. These possibilities may be considered by studying the genetic architecture of responses to male signals and to the environmental stimuli that were purportedly ‘exploited’ by those signals. However, no previous study has addressed the genetic control of sensory exploitation. We investigated this question in an acoustic pyralid moth, Achroia grisella, in which a male ultrasonic song attracts females and perception of ultrasound likely arose in the context of detecting predatory bats. We examined the genetic architecture of female response to bat echolocation signals and to male song via a cartographic study of quantitative trait loci (QTL) influencing these receiver traits. We found several QTL for both traits, but none of them were colocalized on the same chromosomes. These results indicate that – to the extent to which male A. grisella song originated by the process of sensory exploitation – some modification of the female responses occurred since the origin of the male signal.     

Variation and repeatability of ultrasonic sexual advertisement signals inAchroia grisella (Lepidoptera: Pyralidae)

MaleAchroia grisella (Lepidoptera: Pyralidae) produce ultrasonic advertisement signals for pair formation. The signals are generated by wing-fanning and consist of pairs of approximately 100-μs pulses of 70- to 130-kHz sound. In a previous study, playback experiments showed that femaleA. grisella preferred signals whose pulses were louder, longer, and delivered at a higher rate and included longer silent (asynchrony) intervals within pairs. To understand the variation and repeatability of these signal characters, acoustic signals of 18A. grisella males were recorded twice daily on the first 4 days and the seventh day after adult eclosion. ANOVA and MANOVA revealed significant among-individual and among-age variation for all signal characters. Peak amplitude, average amplitude, rate, and pulse length peaked 2–3 days after eclosion and then decreased. Asynchrony interval, however, continued to increase as males aged. Repeatabilities of peak amplitude, average amplitude, rate, and asynchrony interval were all relatively high (>0.5).     

Size-related sexual selection and yeast diet inDrosophila buzzatii (Diptera: Drosophilidae)

Size-related sexual selection (SRSS) was examined on four traits (thorax and wing length and head and face width) inDrosophila buzzatii, by scoring male copulatory status in two mass-mating experiments. Using axenic females, experiment 1 was carried out with axenic males, and experiment 2 with yeast-supplemented males. While there was no indication of SRSS in experiment 1, such selection was substantial in yeast-supplemented males, which transmitted yeasts to mating females. Multivariate analyses of selection indicated that face width is the measured trait on which directional SRSS essentially acted in yeast-supplemented males, resulting in indirect selection on body size. Because this selection was affected by yeast diet in males, its possible interaction with the yeast transmission from males to females during the courtship is discussed.     

Sexual selection on cuticular hydrocarbons of male sagebrush crickets in the wild

Cuticular hydrocarbons (CHCs) play an essential role in mate recognition in insects but the form and intensity of sexual selection on CHCs has only been evaluated in a handful of studies, and never in a natural population. We quantified sexual selection operating on CHCs in a wild population of sagebrush crickets, a species in which nuptial feeding by females imposes an unambiguous phenotypic marker on males. Multivariate selection analysis revealed a saddle-shaped fitness surface, suggesting a complex interplay between the total abundance of CHCs and specific CHC combinations in their influence on female choice. The fitness surface resulting from two axes of disruptive selection reflected a trade-off between short- and long-chained CHCs, suggesting that males may be sacrificing some level of desiccation resistance in favour of increased attractiveness. There was a significant correlation between male body size and total CHC abundance, suggesting that male CHCs provide females with a reliable cue for maximizing benefits obtained from males. Notwithstanding the conspicuousness of males’ acoustic signals, our results suggest that selection imposed on males via female mating preferences may be far more complex than previously appreciated and operating in multiple sensory modalities.     

INBREEDING AND ADVERTISEMENT CALLING IN THE CRICKET TELEOGRYLLUS COMMODUS: LABORATORY AND FIELD EXPERIMENTS

If sexually selected traits reveal a male's heterozygosity or condition to females, then such traits should exhibit declines with inbreeding. We tested this by examining the effect of inbreeding on advertisement calling in male crickets Teleogryllus commodus. We investigated the effect of one generation of full‐sibling mating on calling effort and fine‐scale call structure. Inbreeding reduced calling effort but had no effect on call structure. We then compared the attractiveness of inbred and outbred calls in the field by monitoring how many wild females were attracted to each call type. From the field data, we conducted a selection analysis to identify the major axes of linear and nonlinear multivariate sexual selection on call structure. A comparison of multivariate attractiveness of inbred and outbred calls along each major axis of selection revealed no difference in attractiveness. Our results suggest that inbred male calls have a fine‐scale structure that is no less attractive to females than that of outbred calls. However, because inbred males call less often, and female T. commodus prefer males with a higher calling effort, inbred males will suffer reductions in mating success. Females who base mate choice on call rate are therefore using a signal correlated with male heterozygosity and/or condition.     

CRITERIA OF FEMALE MATE CHOICE IN DROSOPHILA LITTORALIS,D. MONTANA,AND D. EZOANA

We examined sexual selection by Drosophila littoralis, D. montana, and D. ezoana females on male courtship sounds to determine whether the females use absolute or relative criteria when choosing their mates. Behavior of the females was observed, when they were courted by a single male producing normal sounds, or by a single wing-manipulated male producing abnormal sounds; and when they were courted by one or both of these males in a choice situation. The females usually accepted short-winged (but not wingless) males producing abnormal sounds, if they had no alternatives. However, if they heard the sound produced by a normal male, they rejected the deficient male. Drosophila littoralis and D. ezoana females selected between two wing-manipulated males with different wing areas. Our results suggest that the females choose their mates on the basis of relative criteria if the signals emitted by the courting males are within the range of acceptable cues.     

DIRECT AND INDIRECT SEXUAL SELECTION AND QUANTITATIVE GENETICS OF MALE TRAITS IN GUPPIES (POECILIA RETICULATA)

Abstract.— The ornamentation and displays on which sexual attractiveness and thus mating success are based may be complex and comprise several traits. Predicting the outcome of sexual selection on such complex phenotypes requires an understanding of both the direct operation of selection on each trait and the indirect consequences of selection operating directly on genetically correlated traits. Here we report the results of a quantitative genetic analysis of the ornamentation, sexual attractiveness, and mating success of male guppies (Poecilia reticulata). We analyze male ornamentation both from the point of view of single ornamental traits (e.g., the area of each color) and of composite measures of the way the entire pattern is likely to be perceived by females (e.g., the mean and contrast in chroma). We demonstrate that there is substantial additive genetic variation in almost all measures of male ornamentation and that much of this variation may be Y linked. Attractiveness and mating success are positively correlated at the phenotypic and genetic level. Orange area and chroma, the area of a male's tail, and the color contrast of his pattern overall are positively correlated with attractiveness and/or mating success at the phenotypic and genetic levels. Using attractiveness and mating success as measures of fitness, we estimate gradients of linear directional sexual selection operating on each male trait and use equations of multivariate evolutionary change to predict the response of male ornamentation to this sexual selection. From these analyses, we predict that indirect selection may have important effects on the evolution of male guppy color patterns.     

Sexually selected dichromatism in the hihi Notiomystis cincta: multiple colours for multiple receivers

Why do some bird species show dramatic sexual dichromatism in their plumage? Sexual selection is the most common answer to this question. However, other competing explanations mean it is unwise to assume that all sexual dichromatism has evolved by this mechanism. Even if sexual selection is involved, further work is necessary to determine whether dichromatism results from competition amongst rival males, or by female choice for attractive traits, or both. Here, we test whether sexually dichromatic hihi (Notiomystis cincta) plumage is currently under sexual selection, with detailed behavioural and genetic analyses of a free‐living island population. Bateman gradients measured for males and females reveal the potential for sexual selection, whilst selection gradients, relating reproductive success to specific colourful traits, show that there is stabilizing selection on white ear tuft length in males. By correlating colourful male plumage with different components of reproductive success, we show that properties of yellow plumage are most likely a product of male–male competition, whilst properties of the black and white plumage are an outcome of both male–male competition and female choice. Male plumage therefore potentially signals to multiple receivers (rival males and potential mates), and this may explain the multicoloured appearance of one of the most strikingly dichromatic species in New Zealand.     

Independence of Sexual and Anti-Predator Perceptual Functions in an Acoustic Moth: Implications for the Receiver Bias Mechanism in Signal Evolution

The receiver bias model for the evolution of mating signals proposes that selection favors male displays that happen to stimulate a general, ancestral perception in females such that receptivity and successful courtship increase. If these male signals do arise, however, the female perception will operate in two contexts, the original, typically non‐sexual, one and courtship. We may then ask whether these two functions represent the same or distinct traits, which may be under separate neural and genetic control. We studied this question in Achroia grisella, a pyralid moth species in which males attract females, with an ultrasonic mating song. Hearing in pyralid moths is widespread and originated in an anti‐predator context – the perception and avoidance of echolocating bats – and it is inferred that the male song found in A. grisella, and in several other pyralid species, arose subsequently via a receiver bias mechanism: Females perceiving male‐produced ultrasound and responding with anti‐predator behavior normally exhibited in the presence of bat echolocations may have inadvertently increased the likelihood of successful courtship. We measured hearing responses in both sexual and anti‐predator contexts in inbred lines developed from an A. grisella population. Significant inter‐line variance was observed for sensitivity thresholds for female response to male song and for both female and male responses to synthetic bat echolocation signals. Female responses to male song and to synthetic echolocations differed markedly in sensitivity, and the median sexual and anti‐predator responses in the various lines were not correlated. However, a higher level of similarity occurs between the female and male anti‐predator responses. Thus, genetic variance for sexual and anti‐predator responses appears to exist, and the two responses may represent independent traits. These results imply that when male signals originate via a receiver bias mechanism, female perception does not necessarily remain fixed in its ancestral state but has the potential for continued modification.     

FEMALE REPRODUCTIVE EFFORT DEPENDS ON THE DEGREE OF ORNAMENTATION OF THEIR MATES

Sexual selection theory assumes that secondary sexual characters do not influence female reproductive effort. Female animals may invest relatively more in reproduction if they acquire mates of high phenotypic quality, because offspring sired by preferred males may be relatively more viable than offspring sired by less preferred males. Here we report for the first time in a field study that females of the monogamous barn swallow Hirundo rustica adjust their reproductive effort to the attractiveness of their mates. Experimental manipulation of male tail length, which is a trait currently subject to a directional female mating preference, affected the reproductive effort by females in single broods as well as their decision on the seasonal number of clutches. These results, and those of previous experiments, demonstrate that female barn swallows assess the quality of their mates throughout the reproductive season and adjust their reproductive decisions accordingly. This result has important implications for the theory of sexual selection and for the possibility of testing current models of female mate preferences, because the viability of offspring will be confounded by differential reproductive effort.     

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.     

Crowd control: sex ratio affects sexually selected cuticular hydrocarbons in male Drosophila serrata

Although it is advantageous for males to express costly sexually selected signals when females are present, they may also benefit from suppressing these signals to avoid costly interactions with rival males. Cuticular chemical profiles frequently function as insect sexual signals; however, few studies have asked whether males alter these signals in response to their social environment. In Drosophila serrata, an Australian fly, there is sexual selection for a multivariate combination of male cuticular hydrocarbons (CHCs). Here, we show that the ratio of females to males that an adult male experiences has a strong effect on his CHC expression, with female‐biased adult sex ratios eliciting greater expression of CHC profiles associated with higher male mating success. Classical models predict that male reproductive investment should be highest when there is a small but nonzero number of rivals, but we found that males expressed the most attractive combination of CHCs when there were no rivals. We found that male CHCs were highly sensitive to adult sex ratio, with males expressing higher values of CHC profiles associated with greater mating success as the ratio of females to males increased. Moreover, sex ratio has a stronger effect on male CHC expression than adult density. Finally, we explore whether sex ratio affects the variance among a group of males in their CHC expression, as might be expected if individuals respond differently to a given social environment, but find little effect. Our results reveal that subtle differences in social environment can induce plasticity in male chemical signal expression.     

A novel method of comparing mating success and survival reveals similar sexual and viability selection for mobility traits in female tree crickets

The relationship between sexual and viability selection in females is necessarily different than that in males, as investment in sexual traits potentially comes at the expense of both fecundity and survival. Accordingly, females do not usually invest in sexually selected traits. However, direct benefits obtained from mating, such as nuptial gifts, may encourage competition among females and subsidize investment into sexually selected traits. We compared sexual and viability selection on female tree crickets Oecanthus nigricornis, a species where females mate frequently to obtain nuptial gifts and sexual selection on females is likely. If male choice determines female mating success in this species, we expect sexual selection for fecundity traits, as males of many species prefer more fecund females. Alternatively, intrasexual scramble or combat competition on females may select for larger jumping legs or wider heads (respectively). We estimated mating success in wild caught crickets using microsatellite analysis of stored sperm and estimated relative viability by comparing surviving female O. nigricornis to those captured by a common wasp predator. In support of the scramble competition hypothesis, we found sexual selection for females with larger hind legs and narrower heads. We also found stabilizing viability selection for intermediate head width and hind leg size. As predicted, traits under viability and sexual selection were very similar, and the direction of that selection was not opposing. However, because the shape of sexual and viability selection differs, these episodes of selection may favour slightly different trait sizes.     

SEXUAL SELECTION IN A WOLF SPIDER: MALE DRUMMING ACTIVITY,BODY SIZE,AND VIABILITY

Females are often believed to actively choose highly ornamented males (males with extravagant morphological signals or intense sexual display), and ornaments should be honest signals of male viability. However, this belief is relying only on some pieces of empirical evidence from birds. Our study reports active female choice on sexual display that indicates male viability in spiders. We established trials in which we studied female choice in relation to male courtship drumming activity and body size. Females chose the most actively drumming males as mating partners, but the body size of the males did not seem to be selected. Male drumming activity turned out to be a good predictor of male viability, whereas male viability was independent of male body mass. Our results suggest that by actively choosing mates according to male drumming performance, but independently of male body mass, females are preferring viable males as mates. Because Hygrolycosa rubrofasciata males do not provide obvious direct benefits to their offspring, females may gain some indirect benefits; offspring may have higher chance of survival, or the offspring may inherit the attractiveness of their father.     

Measuring sexual selection on females in sex‐role‐reversed Mormon crickets (Anabrus simplex,Orthoptera: Tettigoniidae)

Although many studies examine the form of sexual selection in males, studies characterizing this selection in females remain sparse. Sexual selection on females is predicted for sex‐role‐reversed Mormon crickets, Anabrus simplex, where males are choosy of mates and nutrient‐deprived females compete for matings and nutritious nuptial gifts. We used selection analyses to describe the strength and form of sexual selection on female morphology. There was no positive linear sexual selection on the female body size traits predicted to be associated with male preferences and female competition. Instead, we detected selection for decreasing head width and mandible length, with stabilizing selection as the dominant form of nonlinear selection. Additionally, we tested the validity of a commonly used instantaneous measure of mating success by comparing selection results with those determined using cumulative mating rate. The two fitness measures yielded similar patterns of selection, supporting the common sampling method comparing mated and unmated fractions.     

BREEDING COMPETITION IN A PACIFIC SALMON (COHO: ONCORHYNCHUS KISUTCH): MEASURES OF NATURAL AND SEXUAL SELECTION

In the breeding system of Pacific salmon, females compete for oviposition territories, and males compete to fertilize eggs. The natural selection in females and sexual selection in males likely has been responsible for their elaborate breeding morphologies and the dimorphism between the sexes. We quantified direct-selection intensities during breeding on mature coho salmon (Oncorhynchus kisutch), measured for seven phenotypic characters, including three secondary sexual characters. Wild and sea-ranched hatchery coho were used to enhance the range of phenotypes over which selection could be examined. The fish were allowed to breed in experimental arenas where we could quantify components of breeding success as well as estimate overall breeding success. We found that without competition, natural selection acts only on female body size for increased egg production; there is no detectable selection on males for the phenotypic distribution we used. Under competition, the opportunity for selection increased sixfold among females. Natural selection favored female body size and caudal-peduncle (tail) depth. Increased body size meant increased egg production and access to nesting territories. The caudal peduncle, used in burst swimming and nest digging, influenced both successful egg deposition and nest survival. Increasing density increased competition among females, though it did not significantly intensify natural selection on their characters. In males, competition increased the opportunity for selection 52-fold, which was nine times greater than for females. Sexual selection favored male body size and hooked snout length, both characters directly influencing male access to spawning opportunities. Selection on male body size was also affected significantly by breeding density. The ability of large males to control access to spawning females decreased at higher densities reflecting an increase in the operational sex ratio. Further, the relative success of small males, which could sneak access to spawning females, appeared to increase as that of intermediate-sized males decreased. Such disruptive selection may be responsible for the evolution of alternative reproductive tactics in salmon.     

Sexual and natural selection in the evolution of extended phenotypes: the use of green nesting material in starlings

Although sexual selection is typically considered the predominant force driving the evolution of ritualized sexual behaviours, natural selection may also play an important and often underappreciated role. The use of green aromatic plants among nesting birds has been interpreted as a component of extended phenotype that evolved either via natural selection due to potential sanitary functions or via sexual selection as a signal of male attractiveness. Here, we compared both hypotheses using comparative methods in starlings, a group where this behaviour is widespread. We found that the use of green plants was positively related to male‐biased size dimorphism and that it was most likely to occur among cavity‐nesting species. These results suggest that this behaviour is likely favoured by sexual selection, but also related to its sanitary use in response to higher parasite loads in cavities. We speculate that the use of green plants in starlings may be facilitated by cavity nesting and was subsequently co‐opted as a sexual signal by males. Our results represent an example of how an extended phenotypic component of males becomes sexually selected by females. Thus, both natural selection and sexual selection are necessary to fully understand the evolution of ritualized behaviours involved in courtship.