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.     

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.     

The complexity of mating decisions in stalk‐eyed flies

All too often, studies of sexual selection focus exclusively on the responses in one sex, on single traits, typically those that are exaggerated and strongly sexually dimorphic. They ignore a range of less obvious traits and behavior, in both sexes, involved in the interactions leading to mate choice. To remedy this imbalance, we analyze a textbook example of sexual selection in the stalk‐eyed fly (Diasemopsis meigenii). We studied several traits in a novel, insightful, and efficient experimental design, examining 2,400 male–female pairs in a “round‐robin” array, where each female was tested against multiple males and vice versa. In D. meigenii, females exhibit strong mate preference for males with highly exaggerated eyespan, and so we deliberately constrained variation in male eyespan to reveal the importance of other traits. Males performing more precopulatory behavior were more likely to attempt to mate with females and be accepted by them. However, behavior was not a necessary part of courtship, as it was absent from over almost half the interactions. Males with larger reproductive organs (testes and accessory glands) did not make more mating attempts, but there was a strong tendency for females to accept mating attempts from such males. How females detect differences in male reproductive organ size remains unclear. In addition, females with larger eyespan, an indicator of size and fecundity, attracted more mating attempts from males, but this trait did not alter female acceptance. Genetic variation among males had a strong influence on male mating attempts and female acceptance, both via the traits we studied and other unmeasured attributes. These findings demonstrate the importance of assaying multiple traits in males and females, rather than focusing solely on prominent and exaggerated sexually dimorphic traits. The approach allows a more complete understanding of the complex mating decisions made by both males and females.     

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 flies to support the hypothesis that male eyespan is a signal of meiotic drive. Several stalk-eyed fly species are known to exhibit X-linked meiotic drive. A recent quantitative trait locus analysis in Teleopsis dalmanni found a potential link between variation in male eyespan, a sexually selected ornamental trait, and the presence of meiotic drive. This was based on laboratory populations subject to artificial selection for male eyespan. In this study, we examined the association between microsatellite markers and levels of sex ratio bias (meiotic drive) in 12 wild T. dalmanni populations. We collected two data sets: (a) brood sex ratios of wild-caught males mated to standard laboratory females and (b) variation in a range of phenotypic traits associated with reproductive success of wild-caught males and females. In each case, we typed individuals for eight X-linked microsatellite markers, including several that previously were shown to be associated with male eyespan and meiotic drive. We found that one microsatellite marker was very strongly associated with meiotic drive, whereas a second 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 being associated with more female-biased broods. These results suggest that mate preference for exaggerated male eyespan allows females to avoid mating with males carrying the meiotic drive gene and is thus a potential mechanism for the maintenance and evolution of female mate preference.     

Signalling fitness: larger males sire more offspring. Studies of the stalk-eyed fly Cyrtodiopsis whitei (Diopsidae,Diptera)

Some species of stalk-eyed flies (Diopsidae, Diptera) have a sexual dimorphism of eyespan. For example, Cyrtodiopsis whitei males have much longer eyestalks than females of equal body length. Expression of this trait increases with the bearers' size. The slope of the log-log regression line eyespan versus body length is close to two in males, while in females it is roughly one. Behavioural experiments suggest that male eyespan signals quantitatively a male's strength or attractiveness to a competitor or mate. We used 3 pure strains of C. Whitei, which were distinguished by their different phosphoglucomutase allele outfit. We compared the reproductive success of males of different sizes and found the number of offspring to be directly proportional to body length. Thus eyespan, rising with the square of body length, provides an exaggerated and highly conclusive signal in the advertisement of fitness.     

Experimental evidence that female ornamentation increases the acquisition of sperm and signals fecundity

Mate choice can lead to the evolution of sexual ornamentation. This idea rests on the assumption that individuals with more elaborate ornaments than competitors have higher reproductive success due to gaining greater control over mating decisions and resources provided by partners. Nevertheless, how the resources and quality of sexual partners that individuals gain access to are influenced by the ornamentation of rival individuals remains unclear. By experimentally concealing and subsequently revealing female ornaments to males, we confirm in the fowl, Gallus gallus, that female ornamentation influences male mating decisions. We further show, by manipulating the relative ornament size of females, that when females had larger ornaments than competitors they were more often preferred by males and obtained more sperm, especially from higher quality males, as measured by social status. Males may benefit by investing more sperm in females with larger ornaments as they were in better condition and produced heavier eggs. Female ornament size also decreased during incubation, providing a cue for males to avoid sexually unreceptive females. This study reveals how inter-sexual selection can lead to the evolution of female ornaments and highlights how the reproductive benefits gained from mate choice and bearing ornaments can be dependent upon social context.     

Variation in preference for a male ornament is positively associated with female eyespan in the stalk-eyed fly Diasemopsis meigenii

There is currently much interest in mate preferences for sexual ornaments. However, few studies have focused on individual variation in mate preference despite its importance for the rate and direction of sexual selection. Females of the sexually dimorphic stalk-eyed fly, Diasemopsis meigenii, exhibit an unambiguous rejection response towards unattractive males bearing small ornaments. We investigated individual mate preferences using repeated sequential sampling of female rejection or acceptance responses to a wide range of male ornament phenotypes. We found significant variation in the strength of individual preference. In addition, preference was positively associated with female eyespan, a condition-dependent trait putatively linked to visual acuity.     

The evolution of female preferences for multiple indicators of quality

In a variety of species, females exhibit preferences for multiple male ornaments. Several hypotheses have been proposed to explain this phenomenon. Which, if any, of these hypotheses is the most plausible in general remains largely unresolved based on the available empirical data. Yet theoretical studies conclude that the evolution of preferences for multiple signals of male quality is unlikely, especially when the use of an additional cue in mate choice strongly increases the overall cost of choice. This would imply that most male courtship characters do not reflect the male's genetic quality but instead evolved through Fisherian sexual selection. However, the existing models focus on ornaments that signal overall genetic quality and do not address the possibility that different ornaments provide information about different aspects of quality. Therefore, we develop a model in which the ornaments act as signals for distinct quality components. When the ornaments provide overlapping information about these quality components, we retrieve the results of earlier models. However, when the ornaments provide independent information, preferences for multiple ornaments may evolve, even when exhibiting multiple preferences is costly. We discuss our results in relation to the multiple-message and redundant-signal hypotheses for ornament diversity and identify parallels between Fisherian and good-genes mechanisms for the evolution of multiple ornaments.     

Potential fitness benefits from mate selection in the Atlantic cod (Gadus morhua)

Little evidence of benefits from female mate choice has been found when males provide no parental care or resources. Yet, good genes models of sexual selection suggest that elaborated male sexual characters are reliable signals of mate quality and that the offspring of males with elaborate sexual ornaments will perform better than those of males with less elaborate ornaments. We used cod (Gadus morhua L.), an externally fertilizing species where males provide nothing but sperm, to examine the potential of optimal mate selection with respect to offspring survival. By applying in vitro fertilizations, we crossed eight females with nine males in all possible combinations and reared each of the 72 sib groups. We found that offspring survival was dependent on which female was mated with which male and that optimal mate selection has the potential to increase mean offspring survival from 31.9 to 55.6% (a 74% increase). However, the size of the male sexual ornaments and sperm quality (i.e. sperm velocity and sperm density) could not predict offspring survival. Thus, even if there may be large fitness benefits of mate selection, we might not yet have identified the male characteristics generating high offspring survival.     

Assigning sex to pre-adult stalk-eyed flies using genital disc morphology and X chromosome zygosity

Background  

In stalk-eyed flies (Diopsidae) the eyes and antennae are laterally displaced at the ends of elongated eyestalks. Eyespan and the degree of sexual dimorphism in eyespan vary considerably between species and several sexually dimorphic species show sexual selection through female mate preference for males with exaggerated eyespan. The genes on which selection acts to regulate eyespan remain to be identified. This could be achieved by comparing gene expression during eyestalk development in males and females if the sex of pre-adult flies could be reliably assigned. Here we describe two techniques, one morphological and one microsatellite-based, that identify the sex of stalk-eyed fly larvae and pupae.     

Maintenance of genetic variation in sexual ornaments: a review of the mechanisms

Female preferences for elaborate male sexual traits have been documented in a number of species in which males contribute only genes to the next generation. In such systems, mate choice has been hypothesised to benefit females genetically. For the genetic benefits to be possible there must be additive genetic variation (V(A)) for sexual ornaments, such that highly ornamented males can pass fitter genes on to the progeny of choosy females. Here, I review the mechanisms that can contribute to the maintenance of this variation. The variation may be limited to sexual ornaments, resulting in Fisherian benefits in terms of the increased reproductive success of male progeny produced by choosy females. Alternatively, ornaments may capture V(A) in other life-history traits. In the latter case, "good genes" benefits may apply in terms of improved performance of the progeny of either sex. Some mechanisms, however, such as negative pleiotropy, sexually antagonistic variation or overdominance, can maintain V(A )in ornaments and other life-history traits with little variation in total fitness, leaving little room for any genetic benefits of mate choice. Distinguishing between these mechanisms has consequences not only for the theory of sexual selection, but also for evolution of sex and for biological conservation. I discuss how the traditional ways of testing for genetic benefits can usefully be supplemented by tests detecting benefits resulting from specific mechanisms maintaining V(A )in sexual ornaments.     

A trade-off between reproduction and a condition-dependent sexually selected ornament in the house sparrow Passer domesticus

Reproductive effort was manipulated in a free-living population of house sparrows (Passer domesticus) to investigate the trade-off between reproductive investment and the expression of a condition-dependent sexually selected ornament. Phenotypic plasticity in the expression of this trait was related to the experimentally manipulated size of the brood reared by a male. Males that invested more in current reproduction subsequently became more attractive to females in this population as they showed a preference for males with smaller badges. This supports the argument that direct benefits are a primary focus for mate choice by females. Trade-offs between reproductive effort and the expression of sexual ornaments are a potentially important source of phenotypic variation in both sexual ornaments and life-history traits.     

Male sexual ornament size but not asymmetry reflects condition in stalk-eyed flies

Models of sexual selection predict that females use ornament size to evaluate male condition. It has also been suggested that ornament asymmetry provides females with accurate information about condition. To test these ideas we experimentally manipulated condition in the stalk-eyed fly, Cyrtodiopsis dalmanni, by varying the amount of food available to developing larvae. Males of this species have greatly exaggerated eyestalk length and females prefer to mate with males with wider eyespans. Our experiments show that male ornaments (eyestalks) display a disproportionate sensitivity to condition compared with the homologous character in females, and to non-sexual traits (wing dimensions). In contrast, in neither sex did asymmetry reflect condition either in sexual ornaments or in non-sexual traits. We conclude that ornament size is likely to play a far greater role in sexual selection as an indicator of individual condition than does asymmetry.     

Ejaculate investment and attractiveness in the stalk‐eyed fly,Diasemopsis meigenii

The phenotype‐linked fertility hypothesis proposes that male fertility is advertised via phenotypic signals, explaining female preference for highly sexually ornamented males. An alternative view is that highly attractive males constrain their ejaculate allocation per mating so as to participate in a greater number of matings. Males are also expected to bias their ejaculate allocation to the most fecund females. We test these hypotheses in the African stalk‐eyed fly, Diasemopsis meigenii. We ask how male ejaculate allocation strategy is influenced by male eyespan and female size. Despite large eyespan males having larger internal reproductive organs, we found no association between male eyespan and spermatophore size or sperm number, lending no support to the phenotype‐linked fertility hypothesis. However, males mated for longer and transferred more sperm to large females. As female size was positively correlated with fecundity, this suggests that males gain a selective advantage by investing more in large females. Given these findings, we consider how female mate preference for large male eyespan can be adaptive despite the lack of obvious direct benefits.     

Immune defence,extra-pair paternity,and sexual selection in birds

Secondary sexual characters have been suggested to reliably reflect the ability of individuals to resist debilitating parasites, and females may gain direct or indirect fitness benefits from preferring the most extravagantly ornamented males. Extra-pair paternity provides an estimate of an important component of sexual selection in birds. Species with a high frequency of extra-pair paternity have a variance in realized reproductive success that is greater than the variance in apparent reproductive success, and extra-pair copulations and hence extra-pair paternity by females are often directly associated with the expression of male secondary sexual characters. If sexually dichromatic species have experienced a long period of antagonistic coevolution with their parasites, such species should have evolved larger immune defence organs than sexually monochromatic species. Bird species with sexual dichromatism had larger spleens for their body size than monochromatic species in a comparative analysis. Furthermore, species with a high frequency of extra-pair paternity were sexually dichromatic and had large spleens for their body size. These results are consistent with the hypothesis that females of dichromatic bird species seek extra-pair copulations to obtain indirect fitness benefits in terms of superior resistance of their offspring to virulent parasites.     

Long-term persistence of exaggerated ornaments under Fisherian runaway despite costly mate search

Exaggerated ornaments often evolve due to the mating preferences of the opposite sex. Genetic correlations between preferences and ornaments can lead both traits to elaborate dramatically in tandem, in a process known as ‘Fisherian runaway’. However, in most previous models of Fisherian runaway, elaborate ornaments are not expected to persist when preferences are consistently costly to the choosing sex. In contrast, we show here that exaggerated male ornaments can be maintained long term even when females must pay a cost to choose their mates. Preferences per se are not costly in our model, but females can only act on their preferences by investing resources in mate search. We predict that mate search effort should decrease with the cost of sampling additional mates and increase with the number of possible ornaments that females can choose from. The potential for multiple exaggerated ornaments to coexist depends on subtleties of their cost structure: strict trade-offs (additive costs) favour sequential ornament evolution, whereas looser trade-offs (multiplicative costs) allow for coexistence. Lastly, we show that pleiotropy affecting both ornaments and preferences makes it difficult for Fisherian runaway to initiate, increasing the evolutionary time until ornamentation. Our model highlights the important but neglected role of mate search effort in sexual selection.     

Dual functions of a melanin-based ornament in the common yellowthroat

Melanin-based ornaments often function as signals in male-male competition, whereas carotenoid-based ornaments appear to be important in female mate choice. This difference in function is thought to occur because carotenoid pigments are more costly to produce than melanins and are thus more reliable indicators of male quality. We examined the role of melanin- and carotenoid-based ornaments in male-male competition and female choice in the common yellowthroat Geothlypis trichas, a sexually dichromatic passerine. Males display a black facial mask produced by melanin pigmentation and a bright yellow bib (throat, breast and belly) produced by carotenoid pigmentation. In controlled aviary experiments, mask size was the best predictor of both male-male competition and female mate choice, and, therefore, mask size may be regarded as an ornament of dual function. These dual functions may help to maintain the reliability of mask size as an indicator of male quality, despite the potentially low cost of production. The size of the bib was unrelated to male-male competition or female choice, but there was a tendency for females to prefer males with more colourful bibs. We propose that the black mask is important in competition for territories with other males and for attracting females. Our results highlight the need for more studies of the mechanisms of sexual selection in species with ornaments composed of different pigment types.     

Male red coloration,female mate preference,and sperm longevity in the cyprinid fish Puntius titteya

In recent decades, the link between the exaggeration of male sexual ornaments and ejaculate quality has received much attention. When males with conspicuous sexual ornaments have high-quality ejaculate, females are believed to obtain benefits, such as high fertilization success and offspring with good genes, by choosing mates on the basis of male ornamentation. In this study, we examined the relationships among male body coloration, female mate preference, and sperm longevity in the sexually dichromatic fish Puntius titteya. Males of this species assume a bright red coloration over the entire body, and neither sex invests in the parental care of eggs. In the female preference test, females preferred males with redder body coloration over their counterpart males with duller coloration. In addition, the sperm longevity test indicated that redder males had sperm with greater longevity. These results suggest that the red coloration of males in this species may signal sperm longevity and that females can mate with males with higher quality sperm by choosing redder males.     

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.     

Male mate choice based on ontogenetic colour changes of females in the damselfly <Emphasis Type="Italic">Ischnura senegalensis</Emphasis>

While male mate choice behaviour has been reported in many taxa, little is known about its plasticity and evolutionary consequences. In the damselfly Ischnura senegalensis, females exhibit colour dimorphism (gynomorph and andromorph). The body colour of gynomorphs changed ontogenetically in accordance with sexual maturation, while little change occurred in andromorphs. To test the male mate choice between sexually immature and mature females of both morphs, binary choice experiments were conducted. Virgin males that were reared separately from females after emergence did not show significant preference between sexually immature and mature females for both morphs, indicating that virgin males were unable to discriminate female reproductive status. On the other hand, males that had experienced copulation with gynomorphs preferred sexually mature gynomorphs to sexually immature ones. However, males that had experienced copulation with andromorphs could not discriminate between sexually immature and mature andromorphs, probably due to the absence of significant ontogenetic change in their thoracic colour. Therefore, female body colour is an important cue for males in discriminating between sexual maturation stages. Learned mate discrimination depending on copulation experience might help males to detect potential mates effectively and avoid sexually unreceptive immature female. We finally discuss the adaptive significance of the ontogenetic colour change in females.