Eyespan reflects reproductive quality in wild stalk-eyed flies

Handicap models of sexual selection propose that females use male sexual ornaments as a cue in mate choice because they reflect commodities that increase female fitness, either directly or indirectly. In contrast to studies on vertebrates, most investigations of ornaments in insects and other invertebrate taxa have been conducted under laboratory conditions. There is a pressing need to address questions relating to sexual signalling of quality in natural populations, as the arbitrary and uniform environments found in the laboratory fail to reflect the world under which animals have evolved. We investigated associations between male ornaments (exaggerated eyespan), attractiveness, and reproductive quality in a wild population of the sexually ornamented stalk-eyed fly, Teleopsis dalmanni. We also explored the relationship between eyespan and reproductive quality in females to evaluate the potential for sexually antagonistic selection on eyespan. We show that eyespan is a generic correlate of reproductive quality, acting as a reliable mirror of variation in reproductive fitness in both sexes. Our findings suggest that male ornaments signal commodities that are of interest to females in the natural environment in which they, and mate preferences for them, have evolved. In addition, the covariance between female eyespan and reproductive output suggests that the former may be a reliable cue of quality in its own right. Our data provide important insights into the evolutionary forces that shape the evolution of exaggerated eyespan in wild populations of this species.     

Temperature shock during development fails to increase the fluctuating asymmetry of a sexual trait in stalk-eyed flies.

The fluctuating asymmetry (FA) of bilateral traits is claimed to be a general indicator of environmental stress. Exaggerated sexual ornaments are thought to show elevated levels of FA and a greater response to stress than other traits. Previous work with stalk-eyed flies (Cyrtodiopsis dalmanni) has shown that the FA of the sexual trait (male eye stalks), wing length and wing width were unaffected by a continually applied food stress. Here we tested whether a transient stress (24-h heat shock at 31 degrees C during development) affected the FA of these traits. A second experiment tested the combined stresses of transient heat shock at 31 degrees C with continuous exposure to desiccation. In each experiment, temperature shock reduced the trait size, confirming that the treatments were stressful. However, stress had no effect on the FA of individual traits or the FA summed across all traits. Exposure to the combined stresses significantly elevated mortality and reduced trait size compared to the single-stress regime. However, FA did not differ significantly between flies from the two experiments. We found no evidence that FA in sexual and non-sexual traits reflects transient stress during the development of C. dalmanni.     

Heightened condition dependence is not a general feature of male eyespan in stalk-eyed flies (Diptera: Diopsidae)

Stalk-eyed flies are exemplars of sexual selection leading to the evolution of exaggerated male ornaments (eyespan). In Sphyracephala beccarri, there is no evidence for female mate choice for exaggerated male eyespan and only minor sex differences in eyespan. We used S. beccarri to test whether heightened condition dependence only evolves when male eyespan becomes sexually exaggerated. Male eyespan showed heightened condition dependence under food stress compared with a control trait (wing length). However, female eyespan displayed a similar pattern and there was no sex difference in the degree of increased eyespan sensitivity. The finding that eyespan is a sensitive indicator of food stress, even in an unexaggerated state, suggests that this may have acted as a pre-adaptation to the role of eyespan in sexual signalling in other Diopsid species. These results are consistent with handicap theory and Fisher's view of how sexual selection is initiated.     

Juvenile hormone mediates a trade-off between primary and secondary sexual traits in stalk-eyed flies

Trade-offs between developing body parts may contribute to variation in allometric scaling relationships in a variety of taxa. Experimental evidence indicates that both circulating levels of juvenile hormone (JH) and sensitivities of developing body parts to JH can influence morphology in polyphenic insects. However, the extent to which JH may regulate both the development of traits that scale continuously with body size and trade-offs between these traits is largely unknown. Here, I present evidence that the JH analog methoprene applied to final instar larvae of a stalk-eyed fly (Cyrtodiopsis dalmanni) can induce males to produce larger eye-stalks relative to their body size. Examination of testis growth, sperm transfer, and egg maturation indicates that JH induces a trade-off between eye-span and gonad development in adult males, but not females. Age at sexual maturity was unaffected by larval JH applications to either sex. Collectively, these results are consistent with JH-mediated allocation of resources to eye-span at the expense of testes, and indicate potential costs for the production of an exaggerated trait.     

Male sexual ornament size is positively associated with reproductive morphology and enhanced fertility in the stalk-eyed fly <Emphasis Type="Italic">Teleopsis dalmanni</Emphasis>

Background  

Exaggerated male ornaments and displays often evolve in species where males only provide females with ejaculates during reproduction. Although "good genes" arguments are typically invoked to explain this phenomenon, a simpler alternative is possible if variation in male reproductive quality (e.g. sperm number, ejaculate content, mating rate) is an important determinant of female reproductive success. The "phenotype-linked fertility hypothesis" states that female preference for male ornaments or displays has been selected to ensure higher levels of fertility and has driven the evolution of exaggerated male traits. Females of the stalk-eyed fly Teleopsis dalmanni must mate frequently to maintain high levels of fertility and prefer to mate with males exhibiting large eyespan, a condition-dependent sexual ornament. If eyespan indicates male reproductive quality, females could directly increase their reproductive success by mating with males with large eyespan. Here we investigate whether male eyespan indicates accessory gland and testis length, and then ask whether mating with large eyespan males affects female fertility.     

Evolution of female mating preferences in stalk-eyed flies

Sensory exploitation predicts that female mate preferences existbefore the evolution of exaggerated male ornaments. We testedthis prediction by estimating female preference functions, rematingintervals, and copulation durations for three species of stalk-eyedflies. Two species, Cyrtodiopsis whitei and C dalmanni, exhibitextreme sexual dimorphism in eye span, with eye stalks exceedingbody length in large males. In contrast, C quinqucguttata ofboth sexes possess short eye stalks. Maximum parsimony analysisof 437 basepairs of the 16S mitochondrial ribosomal RNA genefrom 6 Malaysian diopsids reveals that short, sexually monomorphiceye stalks are plesiomorphic in Cyrtodiopsis. Observations ofmultiple copulations by females in paired-choice mating chambersindicated that female C whitei and C. dalmanni exhibit relativepreferences for longer eye stalks such that preference intensityincreases linearly with the difference in eye stalk length betweenmales. Females from the sexually monomorphic species showedno detectable preference for male eye stalk length. Female matingpreferences of bodi sexually dimorphic species exhibited significantrepeatability, as expected if genetic variation underlies thepreference. In addition, female C whitei and C. dalmanni exhibitedshorter copulations, mated more frequently, and rejected fewermating attempts than female C quinqueguttata. Thus, opportunitiesfor sperm competition have increased with acquisition of femalepreferences. We conclude that female sensory bias for maleswith long eye span did not exist in a common ancestor to thesespecies. Instead, female preference and remating propensityeither coevolved with eye span dimorphism or evolved after maleeye stalks elongated.     

Gene duplication, tissue-specific gene expression and sexual conflict in stalk-eyed flies (Diopsidae)

Gene duplication provides an essential source of novel genetic material to facilitate rapid morphological evolution. Traits involved in reproduction and sexual dimorphism represent some of the fastest evolving traits in nature, and gene duplication is intricately involved in the origin and evolution of these traits. Here, we review genomic research on stalk-eyed flies (Diopsidae) that has been used to examine the extent of gene duplication and its role in the genetic architecture of sexual dimorphism. Stalk-eyed flies are remarkable because of the elongation of the head into long stalks, with the eyes and antenna laterally displaced at the ends of these stalks. Many species are strongly sexually dimorphic for eyespan, and these flies have become a model system for studying sexual selection. Using both expressed sequence tag and next-generation sequencing, we have established an extensive database of gene expression in the developing eye-antennal imaginal disc, the adult head and testes. Duplicated genes exhibit narrower expression patterns than non-duplicated genes, and the testes, in particular, provide an abundant source of gene duplication. Within somatic tissue, duplicated genes are more likely to be differentially expressed between the sexes, suggesting gene duplication may provide a mechanism for resolving sexual conflict.     

Beak colouration as a possible sexual ornament in gentoo penguins: sexual dichromatism and relationship to body condition

Gentoo penguins (Pygoscelis papua) have conspicuous red beak spots, the function of which is currently unknown. We hypothesized that beak spots might be sexual ornaments and investigated sexual dichromatism, assortative mating and the possible relationship between beak spot colouration and body condition. Beak colouration was measured with a portable spectroradiometer in 19 breeding pairs of gentoo penguin. Body mass and body mass relative to structural body size were used as estimates of body condition. We found that beak spots were sexually dichromatic, as they were more UV in males and more violet in females, but males and females did not mate assortatively in relation to beak spot colouration. Body condition was strongly related to red colouration in males, with individuals in good condition having redder beaks and individuals in poor condition more orange beaks. The beaks of males in good condition were also brighter. Body condition was not significantly related to beak spot colouration in females, so females might show red beak spots because of genetic correlation with the male trait. These results suggest that the red colour of the beak spot has the potential to be a secondary sexual character in males. Interpretation of the sexual dichromatism in the UV colour will require further knowledge of the capability of gentoo penguins to discriminate small differences in UV wavelengths. In any case, experimental manipulation of beak colouration will be needed to ascertain the role of this trait.     

Baltic amber fossils reveal early evolution of sexual dimorphism in stalk-eyed flies (Diptera: Diopsidae)

A cladistic analysis of 16 species of extant and amber fossil stalk-eyed flies of the family Diopsidae places the fossil †Prosphyracephala succini (Loew) as the sister group of all other Diopsinae, the subfamily in which eye stalks occur. The study is based on a scoring including five old and 23 new finds of †P. succini from Baltic amber, and for the first time allows a morphometric analysis of eye span and various body size parameters in this species. The data indicate that sexual dimorphism of the eye stalks already existed in †Prosphyracephala, suggesting that this feature evolved early in the Diopsinae. Contrary to recent views that the ancestral condition of diopsine eye stalks was monomorphic, the new results suggest that sexual selection was involved in the evolution of eye stalks from the very beginning of the lineage.     

Evolution of genetic variation for condition-dependent traits in stalk-eyed flies

Sexual selection has been proposed to increase genetic variation for condition-dependent ornaments. The condition capture model predicts the genetic variance for a sexually selected trait from the genetic variance in condition and the slope of the relationship between the ornament and condition. Assuming that body size reflects condition we assess the efficacy of this model using six species of stalk-eyed flies (Diopsidae). Prior evidence indicates that male eye span exhibits strong condition dependence and is under sexual selection in sexually dimorphic but not monomorphic species. In contrast, thorax width is weakly related to condition and probably under stabilizing selection. We estimated additive genetic variances for eye span, body length and thorax width from half-sib breeding studies and found that the condition capture model explained 97% of the variation in eye span genetic variance but only 7% of thorax width genetic variance. Comparison of phylogenetically independent contrasts revealed that evolutionary change in male eye span genetic variance is due to evolutionary change in the allometric relationship between eye span and condition: not to evolutionary change in genetic variance for condition. These results suggest that sexual selection can accelerate evolutionary change in condition-dependent male ornaments by increasing the genetic variation available for selection.     

Aerial performance of stalk-eyed flies that differ in eye span

Stalk-eyed flies have eyes placed laterally away from the head on elongated peduncles. The elongation of eye span may increase the energetic cost of flight, reduce flight performance via aerodynamic effects or via increased load, or necessitate compensatory changes in other body dimensions. Body mass and body dimensions were measured to test the hypothesis that elongation of eye span is correlated with increased head mass in two closely related species of stalk-eyed flies. Cyrtodiopsis whitei is sexually dimorphic, with the eye span of larger males exceeding body length. Cyrtodiopsis quinqueguttata is sexually monomorphic with eye span substantially less than body length. Although eye span was significantly longer in C. whitei, head mass did not differ between species after accounting for differences in body mass. C. whitei males had longer wings, heavier thoraxes, and lighter abdomens in relation to body mass than did female C. whitei or C. quinqueguttata of either sex. Three-dimensional tracking of flight paths showed that path velocity and the horizontal component of velocity did not differ according to species or sex, but the long-eyed C. whitei males showed reduced overall aerial performance by flying at shallower ascent angles and reduced vertical velocity. Although increased mass loading does not occur in C. whitei males, increased drag, aerodynamic effects from the wake of the eye stalks, and constrained visual processing are possible mechanisms which could cause their reduced performance. Accepted: 7 June 2000     

Meiotic drive alters sperm competitive ability in stalk-eyed flies.

Meiotic drive results when sperm carrying a driving chromosome preferentially survive development. Meiotic drive should therefore influence sperm competition because drive males produce fewer sperm than non-drive males. Whether meiotic drive also influences the competitive ability of sperm after ejaculation is unknown. Here we report the results from reciprocal crosses that are designed for estimating the sperm precedence of male stalk-eyed flies (Cyrtodiopsis whitei) with or without X-linked meiotic drive. We find that nearly half of all sex-ratio males, as compared with 14% of non-sex-ratio males, fail to produce young in a reciprocal cross. Furthermore, the proportion of progeny sired by a sex-ratio male in a female jointly inseminated by a non-sex-ratio male was less than expected from the number of sperm transferred. These effects are not due to differential sperm storage by females because, after a single mating with a sex-ratio male, all females stored sperm and because two sex-ratio males share paternity after jointly mating with a female. In addition to demonstrating a new mechanism of sperm competition, these results provide insight into the maintenance of sex-ratio polymorphisms. Sex-ratio males have less than one-half the fertility of non-sex-ratio males, as is required in order for frequency-dependent selection on males to produce a stable sex-ratio polymorphism.     

The relative importance of size and asymmetry in sexual selection

Developmental stability reflects the ability of individualsto cope with their environment during ontogeny given their geneticbackground. An inability to cope with environmental and geneticperturbations is reflected in elevated levels of fluctuatingasymmetry and other measures of developmental instability. Bothtrait size and symmetry have been implicated as playing an importantrole in sexual selection, although their relative importancehas never been assessed. We collected information on the relationshipbetween success in sexual competition and size and asymmetry,respectively, to assess the relative importance of these twofactors in sexual selection. Studies that allowed comparisonof the relationships for the same traits' size and symmetryand success in sexual competition constituted the data, whichtotaled 73 samples from 33 studies of 29 species. The averagesample-size weighted correlation coefficients between matingsuccess or attractiveness and size and asymmetry, respectively,were used as measures of effect size in a meta-anatysis. Analysiswas conducted on samples, studies, and species separately. Wefound evidence of an overall larger effect of symmetry at thespecies level of analysis, but similar effects at the sampleor study levels. The difference in effect size for charactersize and character symmetry was larger for secondary sexualcharacters than for ordinary morphological characters at thelevel of analysis of samples. The results lend support to theconclusion that symmetry plays an important general role insexual selection, especially symmetry of secondary sexual characters.     

Low cost of reproduction in female stalk-eyed flies, Cyrtodiopsis dalmanni

We investigated the effect of exposure to males on female longevity and egg production in the stalk-eyed fly, Cyrtodiopsis dalmanni. In this species, females typically mate several times each morning over a lifetime that can span several months. We hypothesised that high costs of mating with males would be incompatible with the life history of this species. We predicted that 1) female longevity costs of exposure to males would be low, and 2) that the magnitude of mating-induced fecundity increases in C. dalmanni, if present, would also be low. We tested the predictions by comparing the longevity and lifetime fecundity of virgin and mated females. In line with prediction 1), the longevity difference between virgin and fully reproductive females was small and of borderline significance. In line with prediction 2), egg production was not significantly higher in females continually exposed to males than for virgin females. Our results suggest that costs of reproduction resulting from exposure to males are low in species that mate promiscuously at high rates.     

Coevolution of sperm and female reproductive tract morphology in stalk-eyed flies

Sperm and female reproductive tract morphology are among the most rapidly evolving characters known in insects. To investigate whether interspecific variation in these traits results from divergent coevolution we examined testis size, sperm length and female reproductive tract morphology for evidence of correlated evolution using 13 species of diopsid stalk-eyed flies. We found that sperm dimorphism (the simultaneous production of two size classes of sperm by individual males) is ancestral and occurs in four genera while sperm monomorphism evolved once and persists in one genus. The length of ''long-sperm'' types, though unrelated to male body or testis size, exhibits correlated evolution with two regions of the female reproductive tract, the spermathecae and ventral receptacle, where sperm are typically stored and used for fertilization, respectively. Two lines of evidence indicate that ''short sperm'', which are probably incapable of fertilization, coevolve with spermathecae. First, loss of sperm dimorphism coincides phylogenetically with reduction or loss of spermathecae. Second, evolutionary change in short-sperm length correlates with change in spermathecal size but not spermathecal duct length or ventral receptacle length. Morphological coevolution between sperm and female reproductive tracts is consistent with a history of female-mediated selection on sperm length.     

Hormonal status and test condition, but not sexual experience, modulate partner preference in female rats

A series of experiments was conducted to determine the contributions of hormonal status, test condition, and sexual experience to the display of partner preference by female rats. Preference for a sexually active male rat over a sexually receptive female rat was assessed in independent groups of female rats tested in a condition limiting physical contact (No Contact) and a condition allowing for sexual interaction (Contact). Although hormonal status and test condition influenced the preference for a sexually active male, repeated testing and sexual experience had no effect. Experiment 1 demonstrated that independent of test condition, preference for the male is stronger in estrogen- and progesterone-primed rats than in rats receiving the vehicle. Moreover, independent of hormone condition, rats tested in the No Contact condition exhibit a stronger preference for the male than rats tested in the Contact condition, reflecting in part the active pacing of mating stimulation by sexually receptive rats tested in the Contact condition. Experiment 2 showed that the overall pattern of partner preference in proestrous and diestrous rats was similar to that observed in ovariectomized, estrogen- and progesterone-primed, and oil-treated rats, respectively. In Experiment 3, rats primed with estrogen alone did not exhibit a preference for the male even though fully receptive. Experiments 4 and 5 demonstrated that sexual experience does not affect the expression of preference for the male in estrogen- and progesterone-primed rats. The present findings demonstrate that the female rat's preference for the male is stable across repeated tests and is not affected by sexual experience. Our results also confirm that gonadal hormones influence the expression of a preference for a sexually active male versus a sexually receptive female and demonstrate that the magnitude of preference is modulated by test conditions.     

Male eyespan size is associated with meiotic drive in wild stalk-eyed flies (Teleopsis dalmanni)

This study provides the first direct evidence from wild populations of stalk-eyed fliesto support the hypothesis that male eyespan is a signal of meiotic drive. Severalstalk-eyed fly species are known to exhibit X-linked meiotic drive. A recent quantitativetrait locus analysis in Teleopsis dalmanni found a potential link betweenvariation in male eyespan, a sexually selected ornamental trait, and the presence ofmeiotic drive. This was based on laboratory populations subject to artificial selectionfor male eyespan. In this study, we examined the association between microsatellitemarkers and levels of sex ratio bias (meiotic drive) in 12 wild T. dalmannipopulations. We collected two data sets: (a) brood sex ratios of wild-caught males matedto standard laboratory females and (b) variation in a range of phenotypic traitsassociated with reproductive success of wild-caught males and females. In each case, wetyped individuals for eight X-linked microsatellite markers, including several thatpreviously were shown to be associated with male eyespan and meiotic drive. We found thatone microsatellite marker was very strongly associated with meiotic drive, whereas asecond showed a weaker association. We also found that, using both independent data sets,meiotic drive was strongly associated with male eyespan, with smaller eyespan males beingassociated with more female-biased broods. These results suggest that mate preference forexaggerated male eyespan allows females to avoid mating with males carrying the meioticdrive gene and is thus a potential mechanism for the maintenance and evolution of femalemate preference.     

Male contest investment changes with male body size but not female quality in the spider Nephila clavipes

Animals use rules to adjust their level of investment in a contest. We evaluate male strategies during contests over females in the golden orb-web spider Nephila clavipes. We tested whether male behaviour changes with female value, and found that contests were similar in intensity and outcome whether the female was a juvenile or adult, virgin or non-virgin, or whether one male had invested sperm in the female. We found evidence that males use a self-assessment strategy when deciding to withdraw from a contest. Loser body size and contestant size difference were correlated with a higher frequency of contest escalation, and fights involving two large males were more likely to escalate than a fight in which one male was small. A multiple regression showed that loser body size had a stronger effect on contest escalation than contestant body size difference. More importantly, the size of the winning male had no effect on contest escalation, a key prediction of a self-assessment strategy. In N. clavipes, body size is the primary factor that determines the outcome of male contests, and males do not appear to assess their opponent or the quality of the resource when deciding to withdraw from the fight.