Good genes and old age: Do old mates provide superior genes?

It has been suggested that female preference for older mates in species without parental care has evolved in response to an alleged higher genetic quality of older individuals. This is based on the widespread assumption that viability selection produces older individuals that are genetically superior to younger individuals. In contrast, we propose that the oldest individuals rarely are genetically superior. Quantitative genetic models of life history evolution indicate that young to intermediately aged individuals are likely to possess the highest breeding values of fitness. This conclusion is based on four arguments: 1) Viability selection on older individuals may decrease or at least not substantially increase breeding values of fitness, because there may exist negative genetic correlations between late-age and early-age life history parameters, 2) Fertility selection is likely to raise the fitness of gametes produced by young individuals more than those produced by old individuals, because the covariance between fertility and fitness often decreases with age, 3) The history of selection on their parents makes younger individuals more fit than older individuals, 4) Germ-line mutations, which are generally deleterious, significantly decrease the breeding value of fitness of an individual throughout its lifespan, especially in males. Therefore, females that mate with the oldest males in a population are doing so for reasons other than to obtain offspring of high genetic quality.     

Good genes, old age and life-history trade-offs

The possibility of using old age of a mate as an indicator of genetic quality is currently controversial. Early verbal models as well as a recent simulation study noted that female choice for old mates is beneficial because longevity indicates viability in the current environment. In contrast, a quantitative genetic model of the relationship between age and breeding value of fitness casts strong doubts on the mechanism. The present analysis shows, however, that these doubts are mainly the result of assuming that all variation among individuals arises from differences in allocation between components of fitness. This neglects the possibility of variability in condition as a whole. Instead, when allowing for persistent variability in condition and assuming optimal reaction norms in allocation, it is shown that correlations between survival and genetic quality or fitness can easily be established at all ages. On the other hand, the results also suggest that the validity of verbal arguments is limited, and counterexamples can be generated where low-quality individuals should invest more in survival. Therefore, resolution of the old age indicator problem requires specification of the constraints acting on life-history characteristics.     

Assortative mating for relatedness in a large naturally occurring population of Drosophila melanogaster

New theoretical work on kin selection and inclusive fitness benefits predicts that individuals will sometimes choose close or intermediate relatives as mates to maximize their fitness. However, empirical examples supporting such predictions are rare. In this study, we look for such evidence in a natural population of Drosophila melanogaster. We compared mating and nonmating individuals to test whether mating was nonrandom with respect to relatedness. Consistent with optimal inbreeding, males were more closely related to their mate than to randomly sampled females. However, all individuals collected mating showed higher relatedness and males were not significantly more related to their mate than to other mating females. We also found a negative relationship between relatedness and fecundity. Our results are consistent with the hypothesis that inclusive fitness benefits may drive inbreeding tolerance despite direct costs to fitness; however, an experimental approach is needed to investigate the link between mate preference and relatedness.     

Male size does not affect the strength of male mate choice for high-quality females in Drosophila melanogaster

Theory predicts that the strength of male mate choice should vary depending on male quality when higher-quality males receive greater fitness benefits from being choosy. This pattern extends to differences in male body size, with larger males often having stronger pre- and post-copulatory preferences than smaller males. We sought to determine whether large males and small males differ in the strength (or direction) of their preference for large, high-fecundity females using the fruit fly, Drosophila melanogaster. We measured male courtship preferences and mating duration to show that male body size had no impact on the strength of male mate choice; all males, regardless of their size, had equally strong preferences for large females. To understand the selective pressures shaping male mate choice in males of different sizes, we also measured the fitness benefits associated with preferring large females for both large and small males. Male body size did not affect the benefits that males received: large and small males were equally successful at mating with large females, received the same direct fitness benefits from mating with large females, and showed similar competitive fertilization success with large females. These findings provide insight into why the strength of male mate choice was not affected by male body size in this system. Our study highlights the importance of evaluating the benefits and costs of male mate choice across multiple males to predict when differences in male mate choice should occur.     

Direct benefits of choosing a high‐fitness mate can offset the indirect costs associated with intralocus sexual conflict

Intralocus sexual conflict generates a cost to mate choice: high‐fitness partners transmit genetic variation that confers lower fitness to offspring of the opposite sex. Our earlier work in the fruit fly, Drosophila melanogaster, revealed that these indirect genetic costs were sufficient to reverse potential “good genes” benefits of sexual selection. However, mate choice can also confer direct fitness benefits by inducing larger numbers of progeny. Here, we consider whether direct benefits through enhanced fertility could offset the costs associated with intralocus sexual conflict in D. melanogaster. Using hemiclonal analysis, we found that females mated to high‐fitness males produced 11% more offspring compared to those mated to low‐fitness males, and high‐fitness females produced 34% more offspring than low‐fitness females. These direct benefits more than offset the reduction in offspring fitness caused by intralocus sexual conflict, creating a net fitness benefit for each sex to pairing with a high‐fitness partner. Our findings highlight the need to consider both direct and indirect effects when investigating the fitness impacts of mate choice. Direct fitness benefits may shelter sexually antagonistic alleles from selection, suggesting a novel mechanism for the maintenance of fitness variation.     

Females avoid manipulative males and live longer

Abstract Female mate choice has been demonstrated in a wide variety of species and is now accepted as an important factor in sexual selection. One of the remaining questions, however, is why females prefer specific males. Do females or their offspring benefit from their choice? Or do females choose mates to minimize costs of mating? Here we show that, in the ovoviviparous cockroach Nauphoeta cinerea, where sexual selection has been well documented, females chose mates to avoid costly male manipulation. Females were partnered with preferred or nonpreferred mates, and fitness of the females measured. We found that females lived longer when they mated with preferred males. Female lifespan depended on the rate at which offspring developed from egg to parturition: slower development led to longer life. We manipulated the male pheromone and showed that the component of the pheromone blend that makes males attractive to females also delayed parturition. Thus, like other aspects of sexual conflict in this species, offspring development and thereby the mother's lifespan depended on exposure of females to specific components of the male pheromone. Males benefit from manipulating offspring development because females with accelerated parturition remained unreceptive whereas females with slower developing offspring readily remated after giving birth to their offspring. Our results suggest a hormone‐like role for the male pheromone in N. cinerea and provide the first direct evidence of mate choice to avoid male manipulation. This study shows that dominant males may not be preferred males if they are manipulating females, why multiple components with contrasting effects can exist in a sexual signal, and emphasizes the complex fitness relationships that can arise in species with sexual conflict.     

Correlates of male mating success in the lekking great snipe (Gallinago media): results from a four-year study

To investigate behavioral or morphological traits importantas mate choice cues, we measured selection differentials (s)as the covariances between each trait and male mating success,and directional selection gradients (J3) from multiple linearregression of the standardized traits on male mating success.Data from two leks in four consecutive years were included,and the annual data were analyzed separately. The main findingsare: (1) the distribution of male mating success proved to beless skewed than those found in many other lekking species,(2) only a few traits yielded significant selection gradients,(3) the importance of age on male mating success changed acrossyears, (4) females may use traits with a high variance as matechoice cues, and (5) individual males achieved similar matingsuccesses between years. Attendance and age were the traitsmost consistently correlated with male mating success, but notraits showed significant selection gradients in all years.Our results indicate that variable sexual selection pressuresexisted between years, but the high correlation found betweenthe mating success of individual males in successive seasonsalso indicates that permanent differences in male traits areimportant. Key words: lek, mate choice, sexual selection.     

INTERACTION-INDEPENDENT SEXUAL SELECTION AND THE MECHANISMS OF SEXUAL SELECTION

Darwin identified explicitly two types of sexual selection, male contests (combat and displays) and female choice, and he devoted the overwhelming majority of his examples to traits that influence the outcome of these interactions. Subsequent treatments of sexual selection have emphasized the importance of intra- and intersexual interactions as sources of sexual selection. However, many traits that are important determinants of mating success influence mating success without necessarily affecting the outcome of intra- and intersexual interactions. Here, I argue that traits can be subject to sexual selection even if they do not affect the outcome of intra- and intersexual interactions. I distinguish two types of sexual selection, interaction-independent and interaction-dependent selection, based on whether variance in mating success is the result of trait-dependent outcomes of interactions between conspecifics. I then use this distinction to construct a framework for classifying types of sexual selection that unifies and expands previously proposed frameworks. Finally, I outline several implications that the concept of interaction-independent sexual selection has for the general theory of sexual selection.     

Multivariate sexual selection on male tegmina in wild populations of sagebrush crickets,Cyphoderris strepitans (Orthoptera: Haglidae)

Although the strength and form of sexual selection on song in male crickets have been studied extensively, few studies have examined selection on the morphological structures that underlie variation in males’ song, particularly in wild populations. Geometric morphometric techniques were used to measure sexual selection on the shape, size and symmetry of both top and bottom tegmina in wild populations of sagebrush crickets, a species in which nuptial feeding by females imposes an unambiguous phenotypic marker on males. The size of the tegmina negatively covaried with song dominant frequency and positively covaried with song pulse duration. Sexual selection was more intense on the bottom tegmen, conceivably because it interacts more freely with the subtegminal airspace, which may play a role in song amplification. An expanded coastal/subcostal region was one of the phenotypes strongly favoured by disruptive selection on the bottom tegmen, an adaptation that may form a more effective seal with the thorax to prevent noise cancellation. Directional selection also favoured increased symmetry in tegminal shape. Assuming more symmetrical males are better able to buffer against developmental noise, the song produced by these males may make them more attractive to females. Despite the strong stabilizing selection documented previously on the dominant frequency of the song, stabilizing selection on the resonator that regulates dominant frequency was surprisingly absent. Nonetheless, wing morphology had an important influence on song structure and appears to be subject to significant linear and nonlinear sexual selection through female mate choice.     

FEMALE PREFERENCE FOR MALE COURTSHIP EFFORT CAN DRIVE THE EVOLUTION OF MALE MATE CHOICE

The evolution of male mate choice is constrained by costs of choice in species with a male‐biased operational sex ratio (OSR). Previous theoretical studies have shown that significant benefits of male choice are required, for example, by mating with more fecund females, in order for these costs to be offset and a male preference to spread. In a series of population genetic models we show the novel effect that male mating preference, expressed as a bias in courtship, can spread when females prefer, and thus are more likely to mate with, males who court more. We explore two female preference functions for levels of male courtship, one representing a threshold and the other a weighted female preference. The basic finding generally holds for both preference functions. However, the preference function greatly affects the spread of a male preference allele after the addition of competing males who can court more in total. Our results thus stress that a thorough understanding of the response of females to male courtship is a critical component to understanding male preference evolution in polygynous species.     

Meta-analysis suggests choosy females get sexy sons more than "good genes"

Female preferences for specific male phenotypes have been documented across a wide range of animal taxa, including numerous species where males contribute only gametes to offspring production. Yet, selective pressures maintaining such preferences are among the major unknowns of evolutionary biology. Theoretical studies suggest that preferences can evolve if they confer genetic benefits in terms of increased attractiveness of sons ("Fisherian" models) or overall fitness of offspring ("good genes" models). These two types of models predict, respectively, that male attractiveness is heritable and genetically correlated with fitness. In this meta-analysis, we draw general conclusions from over two decades worth of empirical studies testing these predictions (90 studies on 55 species in total). We found evidence for heritability of male attractiveness. However, attractiveness showed no association with traits directly associated with fitness (life-history traits). Interestingly, it did show a positive correlation with physiological traits, which include immunocompetence and condition. In conclusion, our results support "Fisherian" models of preference evolution, while providing equivocal evidence for "good genes." We pinpoint research directions that should stimulate progress in our understanding of the evolution of female choice.     

Differential mating success of virgin female katydidsRequena verticalis (Orthoptera: Tettigoniidae)

Male katydids (Orthoptera: Tettigoniidae) invest in offspring through nutrients provided in a large spermatophore. Previous research with Requena verticalishad shown that almost all of the investment of males mating with recently mated (4 days previously) females is in eggs fertilized by the female's previous mate. Thus males are predicted to discriminate against such females as mates. In experiments placing males with both a virgin and a female mated 4–5 days previously, virgin females obtained almost all matings. Although male discrimination of mates was noted in the experiments, there was no evidence that such discrimination was against nonvirgins in both this experiment and one in which a single virgin or mated female was placed with a male. Instead, the results suggest that the differential mating was a result of interfemale competition. The mating advantage held by virgin females over nonvirgins appeared to be lost once the latter had oviposited. Finally, there was no evidence from both single- and paired-female experiments that males preferred larger females as mates.     

Female guppies Poecilia reticulata prefer males that can learn fast

The role of learning ability as a potentially desirable male trait in sexual selection was investigated in the guppy Poecilia reticulata . Mate preference tests and the rate at which a male learnt two mazes were used to determine whether female preference was related to male learning ability. In addition, male body size and saturation of the orange patches were measured. Female preference was found to be related to rate of learning, such that males that learnt the mazes faster were found to be more attractive to females, but was not found to be related to body size or saturation.     

Male swordtails court with an audience in mind

Females are usually considered to be the target of male courtship behaviour. In nature, however, social interactions rarely occur without other observers; thus, it is conceivable that some male courtship behaviours are directed not towards females, but rather towards male rivals. The northern swordtail, Xiphophorus birchmanni, is a freshwater fish found in high densities in natural streams. Males court by swimming close to and in parallel with the female, raising their large sail-like dorsal fin, and quivering briefly. Here, we show that females prefer males that display small dorsal fins to those with large ones, and that males are less aggressive to other males with large dorsal fins. Male swordtails also raise their dorsal fins more frequently when courting in the presence of other males. These results suggest that, despite female avoidance of large dorsal fins, males that raise their fin during courtship benefit by intimidating potential competitors; the intended receivers of this signal are thus males, not females. Intrasexual selection can therefore offset the forces of intersexual selection, even in a courtship display.     

Fixed and dilutable benefits: female choice for good genes or fertility

Benefits accruing to females who exercise mate choice have been defined to be either 'direct' or 'indirect'. We suggest an alternative distinction: benefits can be considered 'fixed', meaning they are on average equal to all females mating with the same male (e.g. good genes' benefits) or 'dilutable', meaning they are shared between females mating with the same male, so that the more mates a male has, the lower the average benefit to each (e.g. fertility benefits or many forms of direct benefit). Using a simple model, we show that this distinction has a major effect on the form of female preference. We predict that mating skew will be far greater in species where the benefits are fixed when compared with those where the benefits are dilutable.     

Female mate choice across mating stages and between sequential mates in flour beetles

Few studies have examined how female premating choice correlates with the outcome of copulatory and post-copulatory processes. It has been shown that polyandrous Tribolium castaneum females discriminate among males before mating based on olfactory cues, and also exert cryptic choice during mating through several mechanisms. This study tested whether a male's relative attractiveness predicted his insemination success during copulation. Bioassays with male olfactory cues were used to rank two males as more and less attractive to females; each female was then mated to either her more attractive male followed by less attractive male, or vice versa. Dissections immediately after second copulations revealed a significantly higher percent of successful inseminations for females that remated with more attractive males compared with those that remated with less attractive males. These results indicate that cryptic female choice during copulation reinforces precopulatory female choice in T. castaneum, and suggest that females could use cryptic choice to trade up to more attractive males, possibly gaining better phenotypic or genetic quality of sires.     

Sexual selection for bright females prevails under light pollution

The functions of sexually selected traits are particularly sensitive to changes in the environment because the traits have evolved to in-crease mating success u...     

Random mating with respect to mating status in the simultaneously hermaphroditic land snail Arianta arbustorum

In promiscuous species with sperm storage, males are expected to show a preference for mating with virgin and young females to reduce the risk of sperm competition. In the simultaneous hermaphrodite land snail Arianta arbustorum, sperm production precedes egg production by 2–4 weeks, resulting in a short period of protandric hermaphroditism before shell growth is completed. In natural populations, copulating pairs involving individuals which have not yet completed shell growth (virgins) have been observed. We ran a series of mate-choice experiments to examine whether virgin and nonvirgin (experienced) individuals of A. arbustorum discriminate between virgin and nonvirgin mating partners. We also assessed the number of sperm delivered to partners with different mating status. Neither virgin nor nonvirgin snails showed any preference for mating with a virgin partner. In all test situations mating was random and the number of sperm delivered was not adjusted to the mating status of the partner. Mating success was mainly determined by the activity of the individual. The random mating pattern does not imply random fertilization of eggs because the presence of a sperm-digesting organ and the morphology of the sperm storage organ allow a selective storage and use of sperm in A. arbustorum.     

Direct detection of male quality can facilitate the evolution of female choosiness and indicators of good genes: Evolution across a continuum of indicator mechanisms

The evolution of mating displays as indicators of male quality has been the subject of extensive theoretical and empirical research for over four decades. Research has also addressed the evolution of female mate choice favoring such indicators. Yet, much debate still exists about whether displays can evolve through the indirect benefits of female mate choice. Here, we use a population genetic model to investigate how the extent to which females can directly detect male quality influences the evolution of female choosiness and male displays. We use a continuum framework that incorporates indicator mechanisms that are traditionally modeled separately. Counter to intuition, we find that intermediate levels of direct detection of male quality can facilitate, rather than impede, the evolution of female choosiness and male displays in broad regions of this continuum. We examine how this evolution is driven by selective forces on genetic quality and on the display, and find that direct detection of male quality results in stronger indirect selection favoring female choosiness. Our results imply that displays maybe more likely to evolve when female choosiness has already evolved to discriminate perceptible forms of male quality. They also highlight the importance of considering general female choosiness, as well as preference, in studies of “good genes.”