Directional Sexual Selection Research Articles

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.

Condition-dependent mate choice in the guppy: a role for short-term food restriction?

Condition-dependent mate choice may alter both the strength and direction of sexual selection within species. In this study, the role of short-term food restriction on the mate choice of female guppies was investigated. Food supply to females was restricted over five days, and their mate choice was tested at five day intervals before, during and after the manipulation, each with their own pair of males. Another set of females were also repeatedly tested, but were not food restricted. Food restriction did not affect the mate choice of treatment females, and the mate choice of treatment and control females did not differ. In addition, the mate choice of both food restricted and control females could not be predicted from the colour patterns of males that individual females were paired with, and the mate choice decisions of individual females were not repeatable. To distinguish whether the lack of a treatment effect on mate choice was due to a lack of female response to the treatment, or to a general lack of repeatability in mate choice at five day intervals, the mate choice of females was repeatedly tested at one day intervals. However, in this study, mate choice at one day intervals was also not predictable from male colour patterns, and mate choice was not repeatable. Nevertheless, a third experiment, based on foraging rather than mate choice trials, showed that females that were food restricted for five days altered their feeding behaviour, indicating the treatment did affect female state. Despite this, there was no evidence that mate choice was affected by short term food restriction, although the lack of repeatability in the mate choice of control females at both one and five day intervals means that it cannot be concluded definitively that this population does not show condition-dependent mate choice based on food availability.

EFFECTS OF NATURAL AND SEXUAL SELECTION ON ADAPTIVE POPULATION DIVERGENCE AND PREMATING ISOLATION IN A DAMSELFLY

The relative strength of different types of directional selection has seldom been compared directly in natural populations. A recent meta-analysis of phenotypic selection studies in natural populations suggested that directional sexual selection may be stronger in magnitude than directional natural selection, although this pattern may have partly been confounded by the different time scales over which selection was estimated. Knowledge about the strength of different types of selection is of general interest for understanding how selective forces affect adaptive population divergence and how they may influence speciation. We studied divergent selection on morphology in parapatric, natural damselfly (Calopteryx splendens) populations. Sexual selection was stronger than natural selection measured on the same traits, irrespective of the time scale over which sexual selection was measured. Visualization of the fitness surfaces indicated that population divergence in overall morphology is more strongly influenced by divergent sexual selection rather than natural selection. Courtship success of experimental immigrant males was lower than that of resident males, indicating incipient sexual isolation between these populations. We conclude that current and strong sexual selection promotes adaptive population divergence in this species and that premating sexual isolation may have arisen as a correlated response to divergent sexual selection. Our results highlight the importance of sexual selection, rather than natural selection in the adaptive radiation of odonates, and supports previous suggestions that divergent sexual selection promotes speciation in this group.

Bursa tract diverticulum in the hermaphroditic land snailArianta arbustorum (Stylommatophora: Helicidae): Morphology, function, and evolutionary implications

A bursa tract diverticulum is widespread in the female part of the hermaphroditic reproductive system of stylommatophoran pulmonates. However, the ultrastructure of the diverticulum is unknown and there is only anecdotal evidence for a spermatophore-dissolving function for this organ. In the present study, we examined the ultrastructure of the diverticulum and investigated histological, histochemical, and morphometric changes at different time intervals after mating in the simultaneously hermaphroditic land snail Arianta arbustorum. The diverticulum in this species of snail is a prominent organ, consisting of a luminal columnar epithelium surrounded by a thick layer of connective tissue. During mating, the diverticulum functions as the site of spermatophore uptake. Within the lumen of the diverticulum the spermatophore wall is dissolved or at least partly broken down. The digested material is taken up by epithelial cells and accumulated in molluscan-specific cells of the connective tissue, the so-called rhogocytes. Subsequent to copulation, the total diameter of the diverticulum increases markedly, reaching a maximum size 12 h after mating, while at the same time the thicknesses of the diverticulum wall and diverticulum epithelium decrease. The length of the diverticulum shows a positive allometry and a high phenotypic variation compared to snail size, which suggests that the diverticulum is under directional sexual selection. We propose that the diverticulum in A. arbustorum has evolved in response to selection pressures imposed by divergent evolutionary interests between male and female function.

Costs of breeding and their effects on the direction of sexual selection

A recent life-history model has challenged the importance of the operational sex ratio and the potential reproductive rates of males and females as the factors most important for the control of sexual selection, arguing that the cost of breeding, interpreted as the probability of dying as a consequence of the current breeding attempt, is the single most important factor that best predicts a mating system. In one species of bushcricket, the mating system can be reversed by resource manipulation. Here, we examine the costs of breeding in this system. Consistent with the model, increased costs of breeding can explain female competition and increased male choosiness under resource limitation. However, this is due to differences in the time required for a breeding attempt, rather than differences in breeding mortality which did not differ between the sexes. In general, males lived longer than females and we discuss the possible reasons behind this pattern of sex-biased non-breeding mortality.

Male tail streamer length predicts fertilization success in the North American barn swallow (Hirundo rustica erythrogaster)

In socially monogamous species, extra-pair paternity has the potential to increase the variance in male reproductive success, thereby affecting the opportunity for sexual selection on male extravagant ornamentation. In the European barn swallow (Hirundo rustica rustica), the tail streamer length is a sexually selected male ornament and an honest indicator of viability. The North American barn swallow (Hirundo rustica erythrogaster) also shows sexual dimorphism in tail streamer length, but whether this trait holds the same signalling function in this subspecies is a controversial issue, and the available literature is presently scarce. Here, we present data on paternity in the North American barn swallow, including a complete sampling of extra-pair sires in four colonies. We analysed how extra-pair paternity affected the variance in male fertilization success and examined whether male tail streamer (i.e. the outermost tail feather) length correlated with fertilization success (n=86 males). Extra-pair paternity constituted 31% of all offspring and significantly increased the variance in male fertilization success. The number of offspring sired by extra-pair males accounted for almost half of the total variance in male fertilization success. Males with naturally long tail streamers had a higher fertilization success than males with shorter tail streamers, and this pattern was mainly caused by a higher extra-pair success for males with long tail streamers. Males with long tail streamers also paired with early breeding females in prime body condition. These results are consistent with the idea that there is directional sexual selection on male tail streamer length, possibly mediated through male extra-pair mating success or the timing of breeding onset.

Female throat ornamentation does not reflect cell-mediated immune response in bluethroats Luscinia s. svecica

The brilliantly coloured throat patch in male bluethroats, Luscinia s. svecica, influences their social mating success and both within- and extra-pair paternity. Female bluethroats are highly variable in their extent of throat coloration, from entirely drab to almost male-like. The ornament in females could be due to a genetic correlation between the sexes. However, it has been shown that male bluethroats prefer brightly coloured females, suggesting that female ornamentation has evolved by direct sexual selection on females through male choice. Males may prefer extravagant traits in females if these reliably signal female quality, such as resistance to disease. We investigated whether variation in the extent of structural and melanin plumage ornamentation in female bluethroats reflects cell-mediated immune response. We caught the females at their nests and measured their immune response as a swelling following a challenge by phytohemagglutinin. An analysis of the data from two years of study revealed that the cell-mediated immune response was not related to female ornamentation. However, the immune response was strongly correlated with female body condition. Thus, our results do not support the hypothesis that female ornament expression signals quality in terms of cell-mediated immunity.

Intraspecific sexual selection on a speciation trait, male coloration, in the Lake Victoria cichlid Pundamilia nyererei

The haplochromine cichlids of Lake Victoria constitute a classical example of explosive speciation. Extensive intra- and interspecific variation in male nuptial coloration and female mating preferences, in the absence of postzygotic isolation between species, has inspired the hypothesis that sexual selection has been a driving force in the origin of this species flock. This hypothesis rests on the premise that the phenotypic traits that underlie behavioural reproductive isolation between sister species diverged under sexual selection within a species. We test this premise in a Lake Victoria cichlid, by using laboratory experiments and field observations. We report that a male colour trait, which has previously been shown to be important for behavioural reproductive isolation between this species and a close relative, is under directional sexual selection by female mate choice within this species. This is consistent with the hypothesis that female choice has driven the divergence in male coloration between the two species. We also find that male territoriality is vital for male reproductive success and that multiple mating by females is common.

Directional sexual selection on chroma and within–pattern colour contrast in Labeotropheus fuelleborni

Speciation via intersexual selection on male nuptial colour pattern is thought to have been a major force in promoting the explosive speciation of African haplochromine cichlids, yet there is very little direct empirical evidence of directional preferences within populations. In this study, we used objective spectrophotometry and analyses based on visual physiology to determine whether females of the Katale population of Labeotropheus fuelleborni, a Lake Malawi haplochromine, prefer males that have higher chroma and more within-pattern colour contrast. In paired male preference tests, female Katale L. fuelleborni showed increasing preferences for males with more relatively saturated colours on their flanks. They also showed increasing preferences for males with relatively higher contrast levels among flank elements. This is the first empirical evidence, to our knowledge, for male colour as a directionally sexually selected trait within a haplochromine cichlid population.

Bat genitalia: allometry, variation and good genes

Male genitalia are typically highly variable across species, for which sexual selection is thought to be responsible. Sexually selected traits characteristically show positive allometry and high phenotypic variation, although genitalia seem to be typified by negative allometry due to stabilizing selection. Additionally, while sexual selection appears to be the primary force responsible for genital evolution, the precise mechanism is unclear, but good-genes selection could be involved. If so, male genital variation should correlate with some male quality measure(s). We investigated the allometry of male Nyctalus noctula genitalia and investigated associations between genital size and three phenotypic measures of male quality (body size, relative body mass, and fluctuating asymmetry (FA)). We found that the penis exhibited positive allometry and high phenotypic variation, and was positively associated with male body size and relative body mass, but not with FA. This pattern is more typical of sexually selected display traits, contrasting with general patterns of genital allometry. The baculum was negatively allometric and was not associated with any quality measure. Our results suggest that the N. noctula penis is under directional sexual selection and is a reliable indicator of male phenotypic quality.

SONG LEARNING ACCELERATES ALLOPATRIC SPECIATION

The songs of many birds are unusual in that they serve a role in identifying conspecific mates, yet they are also culturally transmitted. Noting the apparently high rate of diversity in one avian taxon, the songbirds, in which song learning appears ubiquitous, it has often been speculated that cultural transmission may increase the rate of speciation. Here we examine the possibility that song learning affects the rate of allopatric speciation. We construct a population-genetic model of allopatric divergence that explores the evolution of genes that underlie learning preferences (predispositions to learn some songs over others). We compare this with a model in which mating signals are inherited only genetically. Models are constructed for the cases where songs and preferences are affected by the same or different loci, and we analyze them using analytical local stability analysis combined with simulations of drift and directional sexual selection. Under nearly all conditions examined, song divergence occurs more readily in the learning model than in the nonlearning model. This is a result of reduced frequency-dependent selection in the learning models. Cultural evolution causes males with unusual genotypes to tend to learn from the majority of males around them, and thus develop songs compatible with the majority of the females in the population. Unusual genotypes can therefore be masked by learning. Over a wide range of conditions, learning therefore reduces the waiting time for speciation to occur and can be predicted to accelerate the rate of speciation.

Chromosomal polymorphism, morphometric traits and mating success in Leptysma argentina Bruner (Orthoptera).

The South-American species Leptysma argentina Bruner is polymorphic for a centric fusion between chromosomal pairs 3 and 6 (fusion 3/6). Cytogenetic and morphological studies revealed that fusion 3/6 significantly increases some morphometric variables in males. A selection components study showed that the fusion is positively selected for longevity, the direct effect being exerted on thorax height. Moreover, a unisexual approach revealed that sexual male selection acts by increasing third femur length. In the present study the effect of fusion 3/6 on morphometric variables and the effect of body size and karyotype on mating success in both males and females were analysed through a bisexual approach. Total body length (TL) and third femur length (FL) were significantly larger amongst the fusion carrier females. Besides, the largest females and the carriers of the fusion have increased mating success. The selection differential suggests that directional sexual selection favours the females with increased TL and fusion dosage; however, the selection gradient revealed that none of the variables here analysed is a direct target of sexual selection. The male sexual selection study agrees with previous results, showing the importance of the third pair of legs in male mating success among grasshoppers.

Toward a New Sexual Selection Paradigm: Polyandry, Conflict and Incompatibility (Invited Article)

AbstractDarwin's recognition that male–male competition and female choice could favor the evolution of exaggerated male traits detrimental to survival set the stage for more than a century of theoretical and empirical work on sexual selection. While this Darwinian paradigm represents one of the most profound insights in biology, its preoccupation with sexual selection as a directional evolutionary force acting on males has diverted attention away from the selective processes acting on females. Our understanding of female reproduction has been further confounded by discreet female mating tactics that have perpetuated the illusion of the monogamous female and masked the potential for conflict between the sexes. With advances in molecular techniques leading to the discovery that polyandry is a pervasive mating strategy, recognition of these shortcomings has brought the study of sexual selection to its current state of flux. In this paper, we suggest that progress in two key areas is critical to formulation of a more inclusive, sexual selection paradigm that adequately incorporates selection from the female perspective. First, we need to develop a better understanding of male × female and maternal × paternal genome interactions and the role that polyandry plays in providing females with non‐additive genetic benefits such as incompatibility avoidance. Consideration of these interaction effects influencing natural selection on females is important because they can complicate and even undermine directional sexual selection on males. Secondly, because antagonistic coevolution maintains a balance between opposing sides that obscures the conflict itself, many more experimental evolution studies and interventionist investigations (e.g. gene knockouts) are needed to tease apart male manipulative adaptations and female counter‐adaptations. It seems evident that the divisiveness and controversy that has plagued sexual selection theory since Darwin first proposed the idea has often stalled progress in this important field of evolutionary biology. What is now needed is a more pluralistic and integrative approach that considers natural as well as sexual selection acting on females, incorporates multiple sexual selection mechanisms, and exploits advances in physiology and molecular biology to understand the mechanisms through which males and females achieve reproductive success.

LIFE HISTORY AND THE MALE MUTATION BIAS

Abstract If DNA replication is a major cause of mutation, then those life-history characters, which are expected to affect the number of male germline cell divisions, should also affect the male to female mutation bias (am). We tested this hypothesis by comparing several clades of bird species, which show variation both in suitable life-history characters (generation time as measured by age at first breeding and sexual selection as measured by frequency of extrapair paternity) and in am, which was estimated by comparing Z-linked and W-linked substitution rates in gametologous introns. am differences between clades were found to positively covary with both generation time and sexual selection, as expected if DNA replication causes mutation. The effects of extrapair paternity frequency on am suggests that increased levels of sexual selection cause higher mutation rates, which offers an interesting solution to the paradox of the loss of genetic variance associated with strong directional sexual selection. We also used relative rate tests to examine whether the observed differences in am between clades were due to differences in W-linked or Z-linked substitution rates. In one case, a significant difference in am between two clades was shown to be due to W-linked rates and not Z-linked rates, a result that suggests that mutation rates are not determined by replication alone.

SIGNAL TRAIT SEXUAL DIMORPHISM AND MUTUAL SEXUAL SELECTION IN DROSOPHILA SERRATA

The evolution of sexual dimorphism may occur when natural and sexual selection result in different optimum trait values for males and females. Perhaps the most prominent examples of sexual dimorphism occur in sexually selected traits, for which males usually display exaggerated trait levels, while females may show reduced expression of the trait. In some species, females also exhibit secondary sexual traits that may either be a consequence of a correlated response to sexual selection on males or direct sexual selection for female secondary sexual traits. In this experiment, we simultaneously measure the intersex genetic correlations and the relative strength of sexual selection on males and females for a set of cuticular hydrocarbons in Drosophila serrata. There was significant directional sexual selection on both male and female cuticular hydrocarbons: the strength of sexual selection did not differ among the sexes but males and females preferred different cuticular hydrocarbons. In contrast with many previous studies of sexual dimorphism, intersex genetic correlations were low. The evolution of sexual dimorphism in D. serrata appears to have been achieved by sex-limited expression of traits controlled by genes on the X chromosome and is likely to be in its final stages.

Directional postcopulatory sexual selection revealed by artificial insemination.

Postcopulatory sexual selection comprises both sperm competition, where the sperm from different males compete for fertilization, and cryptic female choice, where females bias sperm use in favour of particular males. Despite intense current interest in both processes as potential agents of directional sexual selection, few studies have attributed the success of attractive males to events that occur exclusively after insemination. This is because the interactions between pre- and post-insemination episodes of sexual selection can be important sources of variation in paternity. The use of artificial insemination overcomes this difficulty because it controls for variation in male fertilization success attributable to the female's perception of male quality, as well as effects due to mating order and the relative contribution of sperm from competing males. Here, we adopt this technique and show that in guppies, when equal numbers of sperm from two males compete for fertilization, relatively colourful individuals achieve greater parentage than their less ornamented counterparts. This finding indicates that precopulatory female mating preferences can be reinforced exclusively through postcopulatory processes occurring at a physiological level. Our analysis also revealed that relatively small individuals were advantaged in sperm competition, suggesting a possible trade-off between sperm competitive ability and body growth.

Sexual selection on multivariate phenotype in wild and mass-reared Ceratitis capitata (Diptera: Tephritidae).

Males with a larger thorax and narrower face were found to be favoured by directional sexual selection in a previous field cage experiment where Ceratitis capitata males from the Seib 6-96 genetic sexing strain competed with wild males from Alto Valle (Patagonia) for the possession of wild females. Targets of sexual selection, however, might differ between wild and laboratory females as a response to adaptation to mass-rearing conditions. To evaluate possible divergences on the targets of sexual selection as a by-product of adaptation to mass-rearing conditions, field cage tests were performed with both wild and laboratory females. To avoid possible bias due to correlation among the measured traits (eye length [EL], face width [FW], head width [HW], and thorax length [TL]), a multivariate analysis was applied. Consistent with the previous experiment, the results indicated that TL and FW are probable targets of directional sexual selection independently of female strain. However, laboratory females were less selective than wild ones. Additionally, correlational sexual selection was detected acting on the multivariate phenotype. The effects of correlational selection overlap with those of directional selection on each single trait. The analysis of mating pair characteristics showed patterns that do not match the expectations for a random mating system. The current analysis indicates that during mating pair formation two processes overlap. On the one hand, sexual selection favours males with larger size (TL) and narrower faces (FW). This effect occurs in both wild and laboratory females. In addition, assortative mating based on both phenotype and origin was also observed.

Tail Length and Mutual Mate Choice in Bearded Tits (Panurus biarmicus)

AbstractDirect sexual selection via mutual mate choice can result in both sexes showing conspicuous traits. We experimentally tested whether this hypothesis can explain tail length in the bearded tit (Panurus biarmicus). In this species, both sexes have a long, graduated tail. Males have, however, a longer tail than females, suggesting perhaps that females are choosier than males in selecting mates. We used two choice set‐ups for each sex: shortened vs. control tail individuals and elongated vs. control tail individuals. We found that direct sexual selection seems to operate differently in the two sexes. In both set‐ups, females spent more time with the male with the longest tail, and they also showed sexual display behaviour only towards these males. Males spent more time with control than with short‐tailed females, but they did not discriminate between control and long‐tailed females. Moreover, males displayed preference towards both short‐ and long‐tailed females. Thus, females preferred long‐tailed males, whereas males did not always prefer long‐tailed females. Our study suggests that mutual mate choice has played a role in the evolution of long tails in bearded tits. It also suggests that the sexual dimorphism in tail length has evolved because mate choice exerts a stronger sexual selection pressure on males than on females.

SURVIVAL RATE OF ADULT BARN SWALLOWS HIRUNDO RUSTICA IN RELATION TO SEXUAL SELECTION AND REPRODUCTION

Sexual selection often affects individuals of the two sexes differently by imposing severe survival costs on individuals of the chosen sex, usually males. These costs may be energetic, physiological, mechanical, or ecological, and they can give rise to sex differences in survival. We studied survival rates of male and female adult Barn Swallows Hirundo rustica in a Danish population during 1984–1998, for the first time using capture–mark–recapture techniques to estimate the consequences of sexual selection for sex differences in survival. Males had slightly, but not significantly, higher survival than females. Females had annual survival estimates that were significantly more variable than those for males. Male annual survival rates were not positively correlated with those of females. Hence, different factors were hypothesized to affect male and female survival rate. Consistent with this prediction we found that annual male survival decreased with increasing annual mean length of the outermost tail feathers, which is a secondary sexual character subject to intense directional sexual selection. Heavier females were more likely to survive. Furthermore, females with long tails survived better than short-tailed females. Since tail length in females is an indicator of female condition, both body mass and tail length relationships suggest that females survive better in years when they are in superior condition. Thus, sexual selection as reflected by differences in tail length of males and females contributes in different ways to survival of male and female Barn Swallows.

Differential adult survival and phenotypic variation in a chromosomally polymorphic population of the grasshopper Sinipta dalmani.

Small size results from homozygosity for the polymorphic M4 inversion in the grasshopper Sinipta dalmani. There is directional sexual selection in males favouring the standard sequence and larger individuals. Here I report differential adult male survival in relation to body size and shape in a chromosomally polymorphic population of S. dalmani. Adult male selection was examined by scoring the same five morphometric traits in two consecutive age classes (young and aged males). Multivariate analysis showed significant differences in size between the two samples so that young males are larger for total, third (3 degrees) femur and thorax lengths while aged males show a phenotypic superiority for the lengths of third (3 degrees) tibia and tegmina. Size-adjusted scores for each trait revealed that there are significant differences between young and aged males in shape. In S. dalmani phenotypic selection associated with male mating success may be explained by means of directional selection on body size, while phenotypic selection connected with differential adult male survival may be related to both size and shape.