Male Sexual Ornaments Research Articles

Courtship and Mate Choice in Fishes: Integrating Behavioral and Sensory Ecology

SYNOPSIS. Sexual selection theory predicts a coevolution between male sexual ornamentation and female preference. The implication of this prediction for sensory ecology is that there should be a tight coupling between the physiology of male signal production and the physiology of female signal reception. Indicator models of sexual selection predict that male ornamentation is correlated with male condition, and that female preference is correlated with male ornamentation. Indicator models of sexual selection have a conceptual overlap with resource acquisition and investment models of behavioral ecology. Empirical studies with fishes, particularlywith guppies ( Poecilia reticulata ) and threespine sticklebacks ( Gasterosteus aculeatus ), suggest a strong connection between acquired resources, male condition, male ornamentation, male courtship, and female preference.

Male display rate reveals ejaculate characteristics in the Trinidadian guppy,Poecilia reticulata.

Previous work (Reynolds and Gross 1992) has demonstrated that mate choice enables female guppies, Poecilia reticulata , to obtain heritable benefits (‘good genes’) for their offspring. It is not yet known whether males also signal their functional fertility, that is, their viability as fathers, to female guppies. Our study tested the hypothesis that a male9s behaviour reveals characteristics of his ejaculate. We uncovered a strong correlation between display rate and sperm number in male guppies derived from two wild Trinidadian populations. This result indicates that information on the functional fertility of potential mates is available to females. However, our investigation also found a significant relationship between the frequency of sneaky mating and sperm number. Female guppies in wild populations, particularly those experiencing a high predation regime, are constantly subjected to sneaky mating attempts. As the males responsible for these sneaky matings have highest reserves of sperm they may have the capacity to undermine female choice. The implications of these findings for sperm competition are discussed.

Testing the functional significance of tail streamers

Studies of the evolution of elaborate ornaments have concentrated on their role in increasing attractiveness to mates. The classic examples of such sexually selected structures are the elongated tails of some bird species. Elongated tails can be divided into three categories: graduated tails, pin tails and streamers. There seems to be little debate about whether graduated and pin tails are ornaments; i.e. costly signals used in mate choice. However, in the case of streamers there is considerable discussion about their function. It has been suggested that tail streamers could be (i) entirely naturally selected, (ii) entirely sexually selected, (iii) partly naturally and partly sexually selected. The prime example of a species with tail streamers is the swallow (Hirundo rustica) in which both sexes have tail streamers. In this paper we discuss the aerodynamic consequences of different types of manipulation of the streamer and/or outer tail feather. We make qualitative predictions about the aerodynamic performance of swallows with manipulated tail streamers; these predictions differ depending on whether streamers have a naturally or sexually selected function. We demonstrate that these hypotheses can only be separated if tail streamers are shortened and changes in aerodynamic performance measured during turning flight.

Evolution of reproductive strategies and male sexual ornaments in poeciliid fishes as inferred by mitochondrial 16 rRNA gene phylogeny

Poeciliid fishes have been widely used as a model system in the study of sexual selection mechanisms. In several species belonging to the genera Xiphophorus and Poecilia males show conspicuous ornaments and use courtship display to obtain female cooperation during mating. Conversely most of the remaining poeciliids are drab and achieve copulation mainly through gonopodial thrusting, a fertilization strategy that bypasses the female's consent. We sequenced a portion of the large (16S) mitochondrial ribosomal RNA gene to estimate the phylogenetic relationships among the five tribes of the subfamily Poeciliinae (ROSEN & BAYLEY 1963) and we used the molecular phylogeny to reconstruct the origin of male ornaments and the evolutionary history of the reproductive strategies in this family. Gambusiini were found to be the basal tribe in the subfamily Poeciliinae. In our phylogeny, Xiphophorus and Poecilia were not closely related thus suggesting that the tribe Poeciliini is not a monophyletic group. Gonopodial thrusting was probably the primitive mating strategy of the poeciliids. Sexual ornaments and elaborate courtship behaviour apparently evolved more recently in the genus Xiphophorus and independently in the genus Poecilia.

Artificial selection for increased comb size and its effects on other sexual characters and viability in Gallus domesticus (the domestic chicken)

The expression of secondary ornaments is often positively correlated with the bearer's condition. So far no study has reported on consequences of directional selection on male sexual ornaments in birds, i.e. it is unknown to what extent male sexual traits are genetically correlated and whether selection for secondary ornaments affects viability. In this study we estimate phenotypic and genotypic parameters of three male sexual traits, namely comb size, spur length and testes mass, by using two different lines of domestic chickens (Gallus domesticus). One of the two lines had been artificially selected for large comb size during nine generations whereas the other line was a randomly mated control line. As a result of the selection, male comb size was almost doubled. Data from the selection line indicate that comb size was negatively genetically correlated with testes mass and spur length. The cockerels from the selection line had accordingly lighter testes and shorter spurs than cockerels from the control line. A simple mate choice experiment with females and males from both lines indicated that preferred males had a larger joint expression of comb size and spur length than nonpreferred males. Data from three different selection lines, all with enlarged comb size, clearly reveal a negative effect of comb size on male viability.

Symmetrical male sexual ornaments, paternal care, and offspring quality

Simultaneous manipulation of tail length and tail asymmetry in male barn swallows (Hirundo rustica) has revealed that females prefer maJes with both long and symmetrical tail ornaments over males with short and asymmetrical ornaments. Fluctuating asymmetry in tail length has a negative effect on the maneuvering ability of male barn swallows, and females may prefer males with symmetrical tail ornaments because they thereby acquire more direct fitness benefits in terms of paternal care. The least preferred males with short tails with high asymmetry performed an absolutely and relatively larger share of feeding of nestlings than the most preferred males. However, the combined feeding rate of the pair was not statistically significantly different between treatment groups. Fully grown tarsus length and body mass of offspring on day 15 did not differ between treatments. These results indicate that females do not prefer males with symmetrical tail ornaments because such males contribute a relatively or absolutely larger share of parental duties. Although these results do not explain the basis of female choice for long and symmetrical tails, the results are consistent with a hypothesis that females of species with biparental care should invest differentially in their offspring relative to the quality of their mates. The results are also consistent with a hypothesis that preferred males have access to mates with superior parenting abilities

Female preference for apparently symmetrical male sexual ornaments in the barn swallow Hirundo rustica

The outermost tail feathers of barn swallows Hirundo rustica apparently reliably signal the quality of males, because individuals with the longest tails have the lowest degree of fluctuating asymmetry (random deviations from symmetry in the otherwise symmetrical tail trait) despite the size of their secondary sexual character. I experimentally tested whether females preferred males with symmetrical tails without altering the aerodynamic properties of birds by painting the tips of the outermost tail feathers with white or black correction fluid. Unmated males were randomly assigned to one of four treatments: (i) asymmetrical tails, where the outermost 20 mm of one tail feather was painted white and the other black; (ii) symmetrical tails where the outermost 10 mm of both tail feathers was painted white (symmetric I); (iii) symmetrical tails where the outermost 20 mm of both tail feathers was painted white (symmetric II); or (iv) controls where the outermost 20 mm of both tail feathers was painted black. The experimental treatment affected the duration of the premating period since it took longer for asymmetrical males to acquire a mate than for either group of symmetrical males or control males. This gave rise to a delayed start of laying among males with apparently asymmetrical tails. The seasonal production of fledglings therefore decreased from control males through males with either symmetrical treatment to males with the asymmetrical treatment. Females therefore pay direct attention to the level of fluctuating asymmetry in secondary sexual characters even when the asymmetry does not affect the aerodynamic properties of males.

Positive genetic correlation between female preference and preferred male ornament in sticklebacks

A NUMBER of population genetics models predict the evolution of male sexual ornaments through female choice1, but their genetic assumptions and predictions have hardly been investigated2,3. A key feature of these models is a positive genetic correlation between male ornaments and female preference for them4. Here I test this prediction at the within-population level with three-spined sticklebacks, Gasterosteus aculeatus, which show conspicuous sexual dichromatisnr. Intense red males are preferred in various situations6–10, but there is great intrapopulational variation in redness both among wild-caught6,10 and among laboratory-bred males11, which is partly environmental6 and may be partly genetic12,13. Also, females show considerable intrapopulational variation in their preference for redder males6,8,9, which is partly environmental8,9. Wild-caught, intense red males and dull males were crossed with a number of females from the same population in a full-sib/half-sib breeding design. Daughters were tested for their preference for more intensely red males, and the sons' coloration was quantified. Both traits showed genetic variation. Also the redness of the sons correlated with the preference for red of their sisters, thus the two traits show positive genetic correlation.

Female swallow preference for symmetrical male sexual ornaments.

Many secondary sexual characters are supposed to have evolved as a response to female choice of the most extravagantly ornamented males, a hypothesis supported by studies demonstrating female preferences for the most ornamented males. Comparative studies of elaborate feather ornaments in birds have shown that (1) ornaments have larger degrees of fluctuating asymmetry (small, random deviations from bilateral symmetry caused by an inability of individuals to cope with environmental and genetic stress during development of a character) than other morphological traits, and (2) the degree of fluctuating asymmetry is often negatively related to the size of the ornament. The negative relationship between ornament asymmetry and size suggests that ornament size reliably reflects male quality because the largest secondary sex traits demonstrate the least degree of fluctuating asymmetry. I manipulated tail length and tail asymmetry independently in male swallows (Hirundo rustica) to determine whether ornament size or asymmetry were used as cues in mate choice. Male swallows with elongated, symmetric tails mated earlier, and enjoyed larger annual reproductive success than did males with shortened tails and increased asymmetry. Females therefore prefer large as well as symmetric ornaments, which suggests that females in their mate choice use ornament asymmetry and size as reliable indicators of male quality.

Fluctuating asymmetry in male sexual ornaments may reliably reveal male quality

Human breasts are larger and more enduring than reproductively necessary. It is thus unclear why this costly, yet conspicuous phenotype has been selected for, or what information they might convey about the underlying quality of the female. Following previous research on fluctuating asymmetry, we postulated that breast symmetry would predict a marker of mucosal immunity (salivary immunoglobulin-A; sIgA). Anthropometric breast measurements were provided by 97 young women. Controlling for Body Mass Index (BMI), breast size, and volume, results demonstrated that breast asymmetry predicted lower sIgA, whereas size and volume did not. Results support the hypothesis that symmetrical female breasts are a cue to underlying immunocompetence.

Viability costs of male tail ornaments in a swallow

MALE sexual ornaments that increase mating success may evolve even when they decrease other components of fitness such as survival1–9. But natural covariation between the apparent level of investment in such ornaments and fitness components such as mating success, fecundity and survival, does not provide incontrovertible evidence that the ornaments are costly, because uncontrolled variables such as overall health5 may affect several components of fitness at the same time10–12. By experimental manipulation of male tail length in the monogamous swallow, Hirundo rustica, however, the effects of tail endorment can be tested directly. I show here that in such experiments, females prefer males with elongated tails over those with shortened tails13, but that males with experimentally elongated tail ornaments captured smaller, less profitable prey than those with shortened tails. Impaired foraging efficiency of tail-elongated males increased the frequency of fault bars in their tail feathers, probably as a result of food deficiency during moult. Males with experimentally elongated tail ornaments also decreased their natural tail size during moult, thereby causing a fitness loss in terms of delayed breeding and a reduced annual production of offspring resulting from reduced sexual attractiveness during the following year.

Female choice selects for male sexual tail ornaments in the monogamous swallow

Male secondary sexual ornaments are widespread among polygynous animals1 where they apparently arise through female choice and differential mating success of males2–5. Darwin1 and Fisher2 suggested that female choice should also select for extravagant male ornaments in monogamous birds because female preference for ornamented males should result in earlier breeding which would increase male reproductive success by enhancing the quality and/or the quantity of offspring raised each year. In such cases female reproductive success should be positively related to body condition6 and a heritable component of the time of breeding should be affected by stabilizing selection7. Female preferences for orna-mented males would be favoured by sexual selection because such choosy females would have a greater probability of bearing orna-mented sons with an increased chance of pairing up early. I report here that in the monogamous swallow, Hirundo rustica, males with experimentally elpngated tail ornaments obtain mates more quickly than males with shorter tails, and enjoy increased reproductive output in one breeding season. Such males are also preferred by females seeking extra-pair-bond copulations. Thus male sexual ornaments may also be maintained by female mate choice in monogamous species.

Diploid models of the handicap principle.

"Fisherian" models of sexual selection by female choice assume that females prefer male characters which are initially advantageous or neutral; character and preference then spread through the population. Once female preference has evolved to a higher frequency, the male character can become more extreme and disadvantageous by the action of some force such as the "super-normal stimulus". By contrast, the "handicap principle" of sexual selection proposes that females should prefer more extreme, disadvantaged males: males who survive the disadvantage of the "handicap" must be fitter in other respects. Previous models of various forms of the "handicap principle" have shown that it is very unlikely to work as an alternative to the "Fisherian process". However, recent haploid models have shown that a "condition-dependent handicap" might evolve. Diploid models show that the "condition-dependent handicap" model does not work. Models of "handicaps" operating together with the "Fisherian process" are also presented. It is inferred that "Fisherian" models are more likely than "handicap" models to account for the evolution of male sexual ornaments, although a "handicap" mechanism may aid the operation of the "Fisherian process".

Female choice selects for extreme tail length in a widowbird

Darwin's1 hypothesis that male secondary sexual ornaments evolve through female preferences is theoretically plausible2–7, but there is little experimental field evidence that such preferences exist8–10. I have studied female choice in relation to male tail length in the long-tailed widowbird, Euplectes progne, and report here that males in which the tail was experimentally elongated showed higher mating success than males having normal or reduced tails. The possibility that intrasexual competition among males maintains the long tail was not supported: males with shortened tails held their territories as long as did other males. These results suggest that the extreme tail length in male long-tailed widowbirds is maintained by female mating preferences.