Male Biases for Male Characteristics in Females in Priapella olmecae and Xiphophorus helleri (Family Poeciliidae)

Preexisting receiver biases can affect the evolution of sexually selected traits once traits favored by such biases arise. Female guayacón olmeca, Priapella olmecae , and green swordtail, Xiphophorus helleri , possess a bias favoring sworded conspecific males, despite phylogenetic evidence that the sexually selected sword expressed by male swordtails arose in Xiphophorus after the divergence of the two genera. In this study, we investigated the state of the bias favoring a sword in male Priapella and Xiphophorus to determine whether males also possess a bias that could operate in an intersexual selection context. Male P. olmecae preferred conspecific females with swords to those without swords. Thus, males and females in this unsworded species appear to share a preexisting bias favoring individuals of the opposite sex with swords. Male X. helleri , however, did not express a bias favoring sworded females; instead, in this species in which the sword is restricted to males, males discriminated against conspecific females with swords. Previous work suggests that female mate choice and male–male competition likely contribute to the maintenance of the sword in X. helleri . The sword may also play a role in sex recognition in swordtails. The absence of a sword preference in male green swordtails could reflect the current function of the sword.     

Covariation between predation risk, body size and fin elaboration in the green swordtail, Xiphophorus helleri

Natural and sexual selection can have either opposing or synergistic effects on the evolution of traits. In the green swordtail Xiphophorus helleri , sexual selection arising from female choice is known to favour larger males and males with longer swords. We examined variation in male and female size and fin morphology among 15 populations that varied in their predation environments. Males and females from populations in which piscivorous fishes were present had longer and deeper bodies than did males and females from populations in which piscivorous fishes were absent. Controlling for a positive effect of body size on sword length, males from populations in which piscivores were present had relatively shorter swords than did males from populations in which piscivores were absent. The associations between morphology and predation environment may be due to direct effects of predation, indirect effects of predation, other sources of selection that covary with predator presence, or other environmental effects on trait expression. These results suggest that while sexual selection favours longer swords, natural selection may have an opposing effect on sword length in populations with predators. Natural selection on body size, however, may act synergistically with sexual selection in populations with predators; both may favour the evolution of larger body size. The body size results for X. helleri contrast with related taxa that have become model systems for the study of life history evolution.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 87–100.     

Hybrid origin of a swordtail species (Teleostei: Xiphophorus clemenciae) driven by sexual selection

The swordlike exaggerated caudal fin extensions of male swordtails are conspicuous traits that are selected for through female choice. Swords are one of only few examples where the hypothesis of a pre-existing bias is believed to apply for the evolution of a male trait. Previous laboratory experiments demonstrated that females prefer males with longer swords and even females from some swordless species show an affiliation for males of sworded species. Earlier phylogenetic studies based on maternally inherited mitochondrial DNA placed the sworded southern swordtail Xiphophorus clemenciae with swordless platies, contradicting its morphology-based evolutionary affinities. The analyses of new nuclear DNA markers now recover its traditional phylogenetic placement with other southern swordtails, suggesting that this species was formed by an ancient hybridization event. We propose that sexual selection through female choice was the likely process of hybrid speciation, by mating of platy females with males of an ancestral swordtail lineage. In artificial crosses of descendent species from the two potential ancestral lineages of X. clemenciae the hybrid and backcross males have swords of intermediate lengths. Additionally, mate choice experiments demonstrate that hybrid females prefer sworded males. These experimental lines of evidence make hybridization through xeno-specific sexual selection by female choice the likely mechanism of speciation.     

Male Courtship Behavior and Weapon Trait as Indicators of Indirect Benefit in the Bean Bug,Riptortus pedestris

Females prefer male traits that are associated with direct and/or indirect benefits to themselves. Male–male competition also drives evolution of male traits that represent competitive ability. Because female choice and male–male competition rarely act independently, exploring how these two mechanisms interact is necessary for integrative understanding of the evolution of sexually selected traits. Here, we focused on direct and indirect benefits to females from male attractiveness, courtship, and weapon characters in the armed bug Riptortus pedestris. The males use their hind legs to fight other males over territory and perform courtship displays for successful copulation. Females of R. pedestris receive no direct benefit from mating with attractive males. On the other hand, we found that male attractiveness, courtship rate, and weapon size were significantly heritable and that male attractiveness had positive genetic covariances with both courtship rate and weapon traits. Thus, females obtain indirect benefits from mating with attractive males by producing sons with high courtship success rates and high competitive ability. Moreover, it is evident that courtship rate and hind leg length act as evaluative cues of female choice. Therefore, female mate choice and male–male competition may facilitate each other in R. pedestris. This is consistent with current basic concepts of sexual selection.     

THE EVOLUTION OF THE SEXUALLY SELECTED SWORD IN XIPHOPHORUS DOES NOT COMPROMISE AEROBIC LOCOMOTOR PERFORMANCE

Sexual selection can increase morphological diversity within and among species. Little is known regarding how interspecific variation produced through sexual selection affects other functional systems. Here, we examine how morphological diversity resulting from sexual selection impacts aerobic locomotor performance. Using Xiphophorus (swordtail fish) and their close relatives (N = 19 species), we examined whether the evolution of a longer sexually selected sword affects critical swimming speed. We also examined the effect of other suborganismal, physiological, and morphological traits on critical swimming speed, as well as their relationship with sword length. In correlation analyses, we found no significant relationship between sword length and critical swimming speed. Unexpectedly, we found that critical swimming speed was higher in species with longer swords, after controlling for body size in multiple regression analyses. We also found several suborganismal and morphological predictors of critical swimming speed, as well as a significant negative relationship between sword length and heart and gill mass. Our results suggest that interspecific variation in sword length is not costly for this aspect of swimming performance, but further studies should examine potential costs for other types of locomotion and other components of Darwinian fitness (e.g., survivorship, life span).     

The role of maternal and paternal effects in the evolution of parental quality by sexual selection

Genetic models of maternal effects and models of mate choice have focused on the evolutionary effects of variation in parental quality. There have been, however, few attempts to combine these into a single model for the evolution of sexually selected traits. We present a quantitative genetic model that considers how male and female parental quality (together or separately) affect the expression of a sexually selected offspring trait. We allow female choice of males based on this parentally affected trait and examine the evolution of mate choice, parental quality and the indicator trait. Our model reveals a number of consequences of maternal and paternal effects. (1) The force of sexual selection owing to adaptive mate choice can displace parental quality from its natural selection optimum. (2) The force of sexual selection can displace female parental quality from its natural selection optimum even when nonadaptive mate choice occurs (e.g. runaway sexual selection), because females of higher parental quality produce more attractive sons and these sons counterbalance the loss in fitness owing to over-investment in each offspring. (3) Maternal and paternal effects can provide a source of genetic variation for offspring traits, allowing evolution by sexual selection even when those traits do not show direct genetic variation (i.e. are not heritable). (4) The correlation between paternal investment and the offspring trait influenced by the parental effects can result in adaptive mate choice and lead to the elaboration of both female preference and the male sexually selected trait. When parental effects exist, sexual selection can drive the evolution of parental quality when investment increases the attractiveness of offspring, leading to the elaboration of indicator traits and higher than expected levels of parental investment.     

Predictors of male insemination success in the mosquitofish (Gambusia holbrooki)

Identifying targets of selection is key to understanding the evolution of sexually selected behavioral and morphological traits. Many animals have coercive mating, yet little is known about whether and how mate choice operates when these are the dominant mating tactic. Here, we use multivariate selection analysis to examine the direction and shape of selection on male insemination success in the mosquitofish (Gambusia holbrooki). We found direct selection on only one of five measured traits, but correlational selection involving all five traits. Larger males with longer gonopodia and with intermediate sperm counts were more likely to inseminate females than smaller males with shorter gonopodia and extreme sperm counts. Our results highlight the need to investigate sexual selection using a multivariate framework even in species that lack complex sexual signals. Further, female choice appears to be important in driving the evolution of male sexual traits in this species where sexual coercion is the dominant mating tactic.     

Changed environmental conditions weaken sexual selection in sticklebacks

Environmental heterogeneity can cause the intensity and direction of selection to vary in time and space. Yet, the effects of human-induced environmental changes on sexual selection and the expression of mating traits of native species are poorly known. Currently, the breeding habitats of the three-spined stickleback Gasterosteus aculeatus are changing in the Baltic Sea because of eutrophication and increased growth of algae. Here we show that enhanced growth of filamentous algae increases the costs of mating by inducing an increase in the time and energy spent on courtship and mate choice. This is not followed by a concomitant increase in mate attraction, but instead the strength of selection on male red nuptial coloration and courtship activity is relaxed. Thus, the high investment into the costly sexually selected traits is maladaptive under the new conditions, and the mating system mediates a negative effect of the environmental change on the population. We attribute these environmentally induced changes in the benefit of the mating traits and in the strength of sexual selection to reduced visibility in dense vegetation. Anthropogenic disturbances hence affect the selection pressures that mould the species, which could have long-term effects on the viability and evolution of the populations.     

Sexual Selection in Black Morph Girardinus metallicus (Pisces: Poeciliidae): Females Can Spot a Winner (But We Cannot)

Male–male competition may interfere with the ability of females to choose mates by interrupting courtship or by favoring highly aggressive males who may damage females during mating attempts. Alternatively, females may benefit by mating with dominant males, and female choice and male–male competition may therefore act in unison. The same traits, including aggressiveness, may indicate male quality to females and to rivals. We investigated sexual selection in the black morph of the endemic Cuban poeciliid fish, Girardinus metallicus, to ascertain the links between morphological and behavioral traits and success in intra‐ and intersexual selection. Males conspicuously exhibit their black ventral surface and gonopodium to females during courtship. Dichotomous choice tests revealed female association preferences for certain males, and those same males were more successful in monopolizing access to females when the fish were allowed to directly interact. Dominant males followed, courted, and copulated with females more than subordinate males within a pair, and it appears that females could either assess dominance based on cues we did not measure, or could influence subsequent mating success by their behavior during the dichotomous choice trials. There was an interaction between black status (i.e., whether the male in each pair had more or less ventral black coloration than the other male in that pair) and dominance, such that low‐black dominant males courted early and then shifted to following females, whereas high‐black dominant males courted far more later in the observation period. These results hint at the importance for sexual selection of the interplay between a static morphological trait (black coloration) and a dynamic behavioral trait (aggressiveness), but the functional significance of the courtship display remains a mystery.     

Body size, symmetry and courtship behavior of Dysdercus maurus Distant (Hemiptera: Pyrrhocoridae)

This study analyses the role of body size and symmetry in the sexual selection and courtship behavior of Dysdercus maurus Distant. Sexual conflicts signaled by coercive mating, female resistance, and pre-copulation fights illustrate the mating system. Male-female struggles were observed in all mating attempts. Females tried to reject males by pushing or running and even by vigorously shaking their bodies, in attempts to dislodge the male from their dorsum. In spite of sexual conflicts during courtship, females actively chose their mates based on morphological and behavioral traits. Larger males with more symmetrical tibiae and longer tarsi that are better copula imposers were more successful in sexual competition. Evidence is presented that sexual conflict and female mate choice should not be mutually excluded.     

Ornaments or offspring: costs to reproductive success restrict sexual selection processes

If, in their partner choice, males seek direct benefits (fecund females), the result will be selection for traits indicating female quality rather than for arbitrary (Fisherian) traits. However, the costs of developing and maintaining the sexually selected traits (ornaments) may reduce the resources available to the female for allocation to reproduction and hence result in lower reproductive success per brood. This hitherto unrecognized fecundity cost of sexually selected traits will constrain both the potency of sexual selection mechanisms and the degree of elaboration of sexually selected traits in females, and can also apply to males which invest in their offspring: sexual selection becomes self-limiting. The fitness implications of these costs are examined for both sexes in a variety of mating and parental care patterns. Sexual selection acting on both sexes may lead to either dimorphism or monomorphism, the latter being the case when the quality indicators chosen by both sexes coincide. Ways of evasion or reduction of these reproductive costs of allocations to sexually selected traits include using different resource components for the ornament and for reproduction, or partitioning the two allocations in time.     

Independent Mating Preferences for Male Body Size and Coloration in Female Trinidadian Guppies

Although females in numerous species generally prefer males with larger, brighter and more elaborate sexual traits, there is nonetheless considerable intra‐ and interpopulation variation in mating preferences amongst females that requires explanation. Such variation exists in the Trinidadian guppy, Poecilia reticulata, an important model organism for the study of sexual selection and mate choice. While female guppies tend to prefer more ornamented males as mates, particularly those with greater amounts of orange coloration, there remains variation both in male traits and female mating preferences within and between populations. Male body size is another trait that is sexually selected through female mate choice in some species, but has not been examined as extensively as body coloration in the guppy despite known intra‐ and interpopulation variation in this trait among adult males and its importance for survivorship in this species. In this study, we used a dichotomous‐choice test to quantify the mating preferences of female guppies, originating from a low‐predation population in Trinidad, for two male traits, body length and area of the body covered with orange and black pigmentation, independently of each other. We expected strong female mating preferences for both male body length and coloration in this population, given relaxation from predation and presumably relatively low cost of choice. Females indeed exhibited a strong preference for larger males as expected, but surprisingly a weaker (but nonetheless significant) preference for orange and black coloration. Interestingly, larger females demonstrated stronger preferences for larger males than did smaller females, which could potentially lead to size‐assortative mating in nature.     

Female disdain for swords in a swordtail fish

Studies of mate choice evolution tend to focus on how female mating preferences are acquired and how they select for greater elaboration of male traits. By contrast, far less is known about how female preferences might be lost or reversed. In swordtail fish Xiphophorus, female preference for the sword ornament is an ancestral trait. Xiphophorus birchmanni, however, is one species that has secondarily lost the sword. Using synthetic animation playback of "virtual" males, we found that female X. birchmanni preferred a swordless conspecific over a sworded heterospecific. Moreover, when offered the choice between a conspecific without a sword and one with a digitally attached sword, females preferred the former. These results suggest female preferences need not always select for elaboration of male traits, and they provide a plausible explanation for the lack of introgression of a sexual trait in a naturally occurring hybrid zone.     

Antagonistic selection on body size and sword length in a wild population of the swordtail fish,Xiphophorus multilineatus: Potential for intralocus tactical conflict

Alternative reproductive tactics (ARTs) have provided valuable insights into how sexual selection and life history trade‐offs can lead to variation within a sex. However, the possibility that tactics may constrain evolution through intralocus tactical conflict (IATC) is rarely considered. In addition, when IATC has been considered, the focus has often been on the genetic correlations between the ARTs, while evidence that the ARTs have different optima for associated traits and that at least one of the tactics is not at its optimum is often missing. Here, we investigate selection on three traits associated with the ARTs in the swordtail fish Xiphophorus multilineatus; body size, body shape, and the sexually selected trait for which these fishes were named, sword length (elongation of the caudal fin). All three traits are tactically dimorphic, with courter males being larger, deeper bodied and having longer swords, and the sneaker males being smaller, more fusiform and having shorter swords. Using measures of reproductive success in a wild population we calculated selection differentials, as well as linear and quadratic gradients. We demonstrated that the tactics have different optima and at least one of the tactics is not at its optimum for body size and sword length. Our results provide the first evidence of selection in the wild on the sword, an iconic trait for sexual selection. In addition, given the high probability that these traits are genetically correlated to some extent between the two tactics, our study suggests that IATC is constraining both body size and the sword from reaching their phenotypic optima. We discuss the importance of considering the role of IATC in the evolution of tactical dimorphism, how this conflict can be present despite tactical dimorphism, and how it is important to consider this conflict when explaining not only variation within a species but differences across species as well.     

A receiver bias in the origin of three-spined stickleback mate choice

Receiver-bias models of signal evolution predict that male sexually selected traits evolve through prior selection for other functions. Female three-spined sticklebacks (Gasterosteus aculeatus) in many populations show a mating preference for males with a red throat and jaw. It has been proposed that this preference evolved because the choice of males with red coloration confers direct and indirect benefits to females in accordance with the Fisher-Zahavi model of sexual selection. We present indirect evidence that the preference is an effect of a receiver bias in the perceptual or cognitive system of G. aculeatus for the colour red, which may have arisen in the context of foraging. In laboratory trials, male and female three-spined and nine-spined sticklebacks (Pungitius pungitius) responded most strongly to red objects outside a mating context. This result demonstrates a correlation between a sexually selected trait and an intrinsic attraction to red objects, and supports the sensory-exploitation model for the evolution of red nuptial coloration in three-spined sticklebacks.     

Sexually selected traits and adult survival: a meta-analysis

Traits correlated with male mating success are likely to be subject to sexual selection. Sexually selected characters are thought to be costly to develop and maintain. If males do not vary their investment in sexual traits in relation to their ability to bear the costs, there should be a negative relationship between male longevity or survival and the expression of sexual traits. In particular, a negative relationship is predicted by pure Fisherian models for the evolution of sexual ornaments. The same should also be true for traits that evolve via pleiotropy (e.g., due to sensory exploitation or bias) with no subsequent evolution of condition dependent modification. We collected information on the relationship between traits correlated with male mating rate and estimates of adult male survivorship or life span. In total we obtained 122 samples from 69 studies of 40 species of bird, spider, insect, and fish. In a meta-analysis we calculated the average sample size weighted correlation between trait expression and adult survival. Analyses at the level of samples, studies, and species revealed significant positive relationships (r = 0.08, 0.10, and 0.13, respectively; all P < 0.001). The unweighted correlation at the species level was r = 0.24. In general, males with larger ornaments or weapons, greater body size, or higher rates of courtship showed greater survivorship or longevity. This finding is inconsistent with pure Fisherian models or other models that do not incorporate condition or quality dependent trait expression. It suggests that male investment in sexually selected traits is not fixed but varies in relation to the ability to pay the underlying costs of expressing these characters. Hence, many secondary sexual characters are likely to be condition dependent in their expression.     

The costs of choice in sexual selection

In Fisher's model of sexual selection female mating preferences are not subject to direct selection but evolve purely because they are genetically correlated with the favoured male trait. But when female choice is costly relative to random mating, for example in energy, time or predation risks, the evolution of female mating preference is subject also to direct selection. With costly female choice the set or line of equilibria found in models of Fisher's process no longer exists. On the line the male trait is under zero net selection, and there is no advantage for a female choosing a male with a more exaggerated character. Therefore any cost to choice causes choosiness to decline. In turn this lowers the strength of sexual selection and the male trait declines as well. So when Fisher's process is the sole force of sexual selection and female choice is costly, only transitory increases in female choice and the preferred male trait are possible. It has often been claimed that exaggerated male characters act as markers or revealers of the genetic quality of potential mates. If females choose their mates using traits that correlate with heritable viability differences then stable exaggeration of both female choice and the preferred male character is possible, even when female choice is costly. The offspring of choosy females have not only a Fisherian reproductive advantage but also greater viability. This suggests that in species with exaggerated male ornamentation, in which female choice is costly, it is likely that female mate choice will be for traits that correlate with male genetic quality.     

Female preference for multi-modal courtship: multiple signals are important for male mating success in peacock spiders

A long-standing goal for biologists has been to understand how female preferences operate in systems where males have evolved numerous sexually selected traits. Jumping spiders of the Maratus genus are exceptionally sexually dimorphic in appearance and signalling behaviour. Presumably, strong sexual selection by females has played an important role in the evolution of complex signals displayed by males of this group; however, this has not yet been demonstrated. In fact, despite apparent widespread examples of sexual selection in nature, empirical evidence is relatively sparse, especially for species employing multiple modalities for intersexual communication. In order to elucidate whether female preference can explain the evolution of multi-modal signalling traits, we ran a series of mating trials using Maratus volans. We used video recordings and laser vibrometry to characterize, quantify and examine which male courtship traits predict various metrics of mating success. We found evidence for strong sexual selection on males in this system, with success contingent upon a combination of visual and vibratory displays. Additionally, independently produced, yet correlated suites of multi-modal male signals are linked to other aspects of female peacock spider behaviour. Lastly, our data provide some support for both the redundant signal and multiple messages hypotheses for the evolution of multi-modal signalling.     

Determinants of reproductive success across sequential episodes of sexual selection in a firefly

Because females often mate with multiple males, it is critical to expand our view of sexual selection to encompass pre-, peri- and post-copulatory episodes to understand how selection drives trait evolution. In Photinus fireflies, females preferentially respond to males based on their bioluminescent courtship signals, but previous work has shown that male paternity success is negatively correlated with flash attractiveness. Here, we experimentally manipulated both the attractiveness of the courtship signal visible to female Photinus greeni fireflies before mating and male nuptial gift size to determine how these traits might each influence mate acceptance and paternity share. We also measured pericopulatory behaviours to examine their influence on male reproductive success. Firefly males with larger spermatophores experienced dual benefits in terms of both higher mate acceptance and increased paternity share. We found no effect of courtship signal attractiveness or pericopulatory behaviour on male reproductive success. Taken together with previous results, this suggests a possible trade-off for males between producing an attractive courtship signal and investing in nuptial gifts. By integrating multiple episodes of sexual selection, this study extends our understanding of sexual selection in Photinus fireflies and provides insight into the evolution of male traits in other polyandrous species.     

Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots

To date, few studies have investigated the effects of inbreeding on sexually selected traits, although inbreeding depression on such traits can play an important role in the evolution and ecology of wild populations. Sexually selected traits such as ornamentation and courtship behaviour may not be primary fitness characters, but selection and dominance coefficients of their mutations will resemble those of traits under natural selection. Strong directional selection, for instance, through female mate-choice, purges all but the most recessive deleterious mutations, and the remaining dominance variation will result in inbreeding depression once populations undergo bottlenecks. We analysed the effects of inbreeding on sexually selected traits (colour pattern and courtship behaviour) in the male guppy, Poecilia reticulata, from Trinidad, and found a significant decline in the frequency of mating behaviour and colour spots. Such effects occurred although the genetic basis of these traits, many of which are Y-linked and hemizygous, would be expected to leave relatively little scope for inbreeding depression. Findings suggest that these sexually selected traits could reflect the genetic condition or health of males, and thus may be informative mate-cue characters for female choice as suggested by the 'good genes' model.