Females increase offspring heterozygosity and fitness through extra-pair matings

Females in a variety of species commonly mate with multiple males, and there is evidence that they benefit by producing offspring of higher genetic quality; however, the nature of these genetic benefits is debated. Enhanced offspring survival or quality can result from intrinsic effects of paternal genes---'good genes'--or from interactions between the maternal and paternal genomes--'compatible genes'. Evidence for the latter process is accumulating: matings between relatives lead to decreased reproductive success, and the individual level of inbreeding--measured as average heterozygosity--is a strong fitness predictor. Females should thus benefit from mating with genetically dissimilar males. In many birds, social monogamy restricts mate choice, but females may circumvent this by pursuing extra-pair copulations. Here we show that female blue tits, Parus caeruleus, increase the heterozygosity of their progeny through extra-pair matings. Females thereby produce offspring of higher reproductive value, because less inbred individuals have increased survival chances, a more elaborate male secondary sexual trait (crown colour) and higher reproductive success. The cost of inbreeding may therefore be an important factor driving the evolution of female extra-pair mating.     

Sexual selection and the maintenance of sexual reproduction

The maintenance of sexual reproduction is a problem in evolutionary theory because, all else being equal, asexual populations have a twofold fitness advantage over their sexual counterparts and should rapidly outnumber a sexual population because every individual has the potential to reproduce. The twofold cost of sex exists because of anisogamy or gamete dimorphism-egg-producing females make a larger contribution to the zygote compared with the small contribution made by the sperm of males, but both males and females contribute 50% of the genes. Anisogamy also generates the conditions for sexual selection, a powerful evolutionary force that does not exist in asexual populations. The continued prevalence of sexual reproduction indicates that the 'all else being equal' assumption is incorrect. Here I show that sexual selection can mitigate or even eliminate the cost of sex. If sexual selection causes deleterious mutations to be more deleterious in males than females, then deleterious mutations are maintained at lower equilibrium frequency in sexual populations relative to asexual populations. The fitness of sexual females is higher than asexuals because there is no difference in the fecundity of sexual females and asexuals of the same genotype, but the equilibrium frequency of deleterious mutations is lower in sexual populations. The results are not altered by synergistic epistasis in males.     

Post-mating clutch piracy in an amphibian

Female multiple mating and alternative mating systems can decrease the opportunity for sexual selection. Sperm competition is often the outcome of females mating with multiple males and has been observed in many animals, and alternative reproductive systems are widespread among species with external fertilization and parental care. Multiple paternity without associated complex behaviour related to mating or parental care is also seen in simultaneously spawning amphibians and fishes that release gametes into water. Here we report 'clutch piracy' in a montane population of the common frog Rana temporaria, a reproductive behaviour previously unknown in vertebrates with external fertilization. Males of this species clasp the females and the pair deposits one spherical clutch of eggs. No parental care is provided. 'Pirate' males search for freshly laid clutches, clasp them as they would do a female and fertilize the eggs that were left unfertilized by the 'parental' male. This behaviour does not seem to be size-dependent, and some males mate with a female and perform clutch piracy in the same season. Piracy affected 84% of the clutches and in some cases increased the proportion of eggs fertilized, providing direct fitness benefits both for the pirate males and the females. Sexual selection--probably caused by a strong male-biased sex ratio--occurs in this population, as indicated by size-assortative mating; however, clutch piracy may reduce its impact. This provides a good model to explore how alternative mating strategies can affect the intensity of sexual selection.     

Polyandrous females avoid costs of inbreeding.

Why do females typically mate with more than one male? Female mating patterns have broad implications for sexual selection, speciation and conflicts of interest between the sexes, and yet they are poorly understood. Matings inevitably have costs, and for females, the benefits of taking more than one mate are rarely obvious. One possible explanation is that females gain benefits because they can avoid using sperm from genetically incompatible males, or invest less in the offspring of such males. It has been shown that mating with more than one male can increase offspring viability, but we present the first clear demonstration that this occurs because females with several mates avoid the negative effects of genetic incompatibility. We show that in crickets, the eggs of females that mate only with siblings have decreased hatching success. However, if females mate with both a sibling and a non-sibling they avoid altogether the low egg viability associated with sibling matings. If similar effects occur in other species, inbreeding avoidance may be important in understanding the prevalence of multiple mating.     

Mate choice on fallow deer leks

Leks, on which males defend small clustered mating territories, may have evolved because of the unusual opportunities they provide for female choice of mating partners, and several studies of lek-breeding animals have demonstrated correlations between the mating success of males and their phenotype or behaviour. However, these could arise because (1) females select mates on the basis of male phenotypic traits; (2) males interfere with each other's mating attempts; or (3) females show preferences for particular mating territories, and larger or stronger males are more likely to win access to these territories. Here we report that when fallow bucks on a traditional lek were experimentally induced to change their territories, differences in the mating success of bucks persisted, whereas differences in the position of their territories relative to the centre of the lek did not. The observation that bucks rarely interfered with their neighbours' harems and females moved freely between bucks suggests that females choose their mates on the basis of male phenotype rather than territory type or location. In this population, the immediate factor affecting the movements of females between males was the size of a buck's harem.     

Female choice selects for a viability-based male trait in pheasants

Recent theory on sexual selection suggests that females in species without paternal care choose mates by their secondary sexual characters because these indicate genotypic quality which will be transmitted to the offspring. These ideas are not yet empirically supported as data quantifying the relationship between female mate choice and female reproductive success are lacking. Only in one case, in Colias butterflies, has it been demonstrated unequivocally that females choose 'good genotypes' as mates and there is only one study, on Drosophila, demonstrating that mate choice increases one component of offspring fitness. Spur length of male pheasants (Phasianus colchicus) correlates with various fitness-related properties. We here present the first experimental field data showing that female pheasants select mates on the basis of male spur length and that female mate choice correlates with female reproductive success.     

Rapid evolution of reproductive barriers driven by sexual conflict

A growing amount of experimental data indicates extremely rapid evolution of traits and proteins related to fertilization in many diverging taxa. These data come from studies of sperm or pollen competition between closely related species, and from molecular studies of fertilization proteins. The positive selection for evolutionary novelty that appears to be acting on fertilization systems seems paradoxical because successful reproduction requires the close matching of female and male traits. It has been suggested that perpetual coevolution between the sexes can result from sexual conflict in mating. Sexual conflict occurs when characteristics that enhance the reproductive success of one sex reduce the fitness of the other sex. Numerous examples of sexual conflict resulting from sensory exploitation, polyspermy and the cost of mating have been discussed in detail. The potential for coevolution due to such conflict has been evaluated experimentally. Here I develop a simple mathematical model describing coevolutionary dynamics of male and female traits involved in reproduction. The model shows that continual change in such traits at a constant speed is expected whenever females (or eggs) experience fitness loss from having too many compatible males (or sperms). The plausibility of runaway coevolution increases with increasing population size. Rapid evolution of reproductive barriers driven by sexual conflict may explain increased speciation rates after colonization of new habitats ('adaptive radiation') and high species richness in resource-rich environments.     

Female mating bias results in conflicting sex-specific offspring fitness

Indirect-benefit models of sexual selection assert that females gain heritable offspring advantages through a mating bias for males of superior genetic quality. This has generally been tested by associating a simple morphological quality indicator (for example, bird tail length) with offspring viability. However, selection acts simultaneously on many characters, limiting the ability to detect significant associations, especially if the simple indicator is weakly correlated to male fitness. Furthermore, recent conceptual developments suggest that the benefits gained from such mating biases may be sex-specific because of sexually antagonistic genes that differentially influence male and female reproductive ability. A more suitable test of the indirect-benefit model would examine associations between an aggregate quality indicator (such as male mating success) and gender-specific adult fitness components, under the expectation that these components may trade off. Here, we show that a father's mating success in the cricket, Allonemobius socius, is positively genetically correlated with his son's mating success but negatively with his daughter's reproductive success. This provides empirical evidence that a female mating bias can result in sexually antagonistic offspring fitness.     

Captivity masks inbreeding effects on male mating success in butterflies

Small isolated populations are frequently genetically less diverse than core populations, resulting in higher homozygosity that can hamper their long-term survival. The decrease in fitness of organisms owing to matings between relatives is well known from captive and laboratory animals. Such inbreeding can have strongly deleterious effects on life-history traits and survival, and can be critical to the success of population conservation. Because pedigrees are hard to follow in the wild, most field studies have used marker loci to establish that fitness declines with increasing homozygosity. Very few have experimentally explored the effects of inbreeding in the wild, or compared observations in the laboratory with field conditions. Here, using a technique involving the transfer of marker dusts during copulation, we show that a small decrease in mating success of captive inbred male butterflies in cages is greatly accentuated in conditions with unconstrained flight. Our results have important implications for conservation and for studies of sexual selection because they show that the behaviours underlying patterns of mating can be profoundly influenced by a history of inbreeding or by any restraining experimental conditions.     

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.     

Mutual mate choice in the Asiatic toad, Bufo gargarizans, exerts stabilizing selection on body size

Sexual selection is critical to both reproduction and evolution.The effects of male–male competition and female choice regarding body size have been examined in a large number of taxa,including toad species.Males and females have different optimal reproductive strategies,achieving breeding advantages in discrepant ways.Further,the relative contributions of intra-and inter-sexual size selection vary among species.Thus,to understand the mechanisms affecting mating success,it is important to consider both male–male and male–female interactions simultaneously and elucidate their interrelationship.In this study,we measured body sizes of all mated and unmated individuals in a population of Asiatic toad(Bufo gargarizans)and counted fertilized eggs of several clutches.Based on correlation and regression techniques,we tested for female choice and intra-sexual competition among males relative to body size gradients,and we compared the relative importance of these two processes for mating success.Our results reveal that male–male competition and female choice simultaneously contribute to sexual selection in toads.Furthermore,both interactions are most intense among smaller toads.The synergistic trends of male–male competition and female choice support the mutual mate choice hypothesis and works to stabilize body size in B.gargarizans.Normal distributions of breeding success relative to body size were detected for both sexes,suggesting that medium-sized individuals enjoy a reproductive advantage in the population studied.     

Learning and memory mutations impair acoustic priming of mating behaviour in Drosophila

The courtship song in Drosophila melanogaster has two components, a low-frequency hum and a train of pulses with a species-specific interpulse interval (IPI) of 30-40 ms(1,2). The IPIs oscillate rhythmically, with periods between 50 and 60 s in wild-type males(3). When females are stimulated with artificial songs in the presence of courting but silent (wingless) males, the 'pulse song' and its oscillation can enhance mating success(4?6). If separated males and females are first simultaneously primed with invariant 34-ms IPIs, their subsequent mating success is improved(7). However, exclusive prestimulation of females leads to faster mating only when the hum component of the song is applied, not constant 34-ms IPIs(5). We have re-examined these findings by testing whether prior exposure of females to a rhythmic pulse song speeds up subsequent mating performance. We report here that it does. Furthermore, learning and memory mutations(8), expressed in the females to whom songs are being played, either 'block' or attenuate the effectiveness of acoustical priming.     

Evidence that sensory traps can evolve into honest signals

Conventional models explaining extreme sexual ornaments propose that these reflect male genetic quality or are arbitrary results of genetic linkage between female preference and the ornament. The chase-away model emphasizes sexual conflict: male signals attract females because they exploit receiver biases. As males gain control of mating decisions, females may experience fitness costs through suboptimal mating rates or post-copulatory exploitation. Elaboration of male signals is expected if females increase their response threshold to resist such exploitation. If ornaments target otherwise adaptive biases such as feeding responses, selection on females might eventually separate sexual and non-sexual responses to the signal. Here we show that the terminal yellow band (TYB) of several Goodeinae species evokes both feeding and sexual responses; sexual responsiveness phylogenetically pre-dates the expression of the TYB in males and is comparable across taxa, yet feeding responsiveness decreases in species with more elaborated TYBs. Displaying a TYB is costly, and thus provides an example where a trait arose as a sensory trap but has evolved into an honest signal.     

Sexual reproduction selects for robustness and negative epistasis in artificial gene networks

The mutational deterministic hypothesis for the origin and maintenance of sexual reproduction posits that sex enhances the ability of natural selection to purge deleterious mutations after recombination brings them together into single genomes. This explanation requires negative epistasis, a type of genetic interaction where mutations are more harmful in combination than expected from their separate effects. The conceptual appeal of the mutational deterministic hypothesis has been offset by our inability to identify the mechanistic and evolutionary bases of negative epistasis. Here we show that negative epistasis can evolve as a consequence of sexual reproduction itself. Using an artificial gene network model, we find that recombination between gene networks imposes selection for genetic robustness, and that negative epistasis evolves as a by-product of this selection. Our results suggest that sexual reproduction selects for conditions that favour its own maintenance, a case of evolution forging its own path.     

基于SSR分子标记检测褐飞虱交配次数及性选择

为探明褐飞虱交配次数和性选择的生殖行为特征,构建了褐飞虱生物型1和生物型Y的近交系,筛选了在不同近交系之间存在明显差异的9个SSR(Simple Sequence Repeats)分子标记用于亲子鉴定.在雌虫交配次数试验中,观察并分子鉴定到23头成功交配的雌虫,其中19头雌虫一生仅进行1次交配,4头雌虫一生进行了2次交...     

Negative genetic correlation between male sexual attractiveness and survival

Indirect selection of female mating preferences may result from a genetic association between male attractiveness and offspring fitness. The offspring of attractive males may have enhanced growth, fecundity, viability or attractiveness. However, the extent to which attractive males bear genes that reduce other fitness components has remained unexplored. Here I show that sexual attractiveness in male guppies (Poecilia reticulata) is heritable and genetically correlated with ornamentation. Like ornamentation, attractiveness may be substantially Y-linked. The benefit of mating with attractive males, and thus having attractive sons, is opposed by strong negative genetic correlation between attractiveness and both offspring survival and the number of sons maturing. Such correlations suggest either antagonistic pleiotropy between attractiveness and survival or linkage disequilibrium between attractive and deleterious alleles. The presence of many colour pattern genes on or near the non-recombining section of the Y chromosome may facilitate the accumulation of deleterious mutations by genetic hitchhiking. These findings show that genes enhancing sexual attractiveness may be associated with pleiotropic costs or heavy mutational loads.     

Roaring by red deer stags advances the date of oestrus in hinds

Some male mammals call loudly and repeatedly during the breeding season. Although the song of male birds is known to have effects on male-male competition, mate selection and ovulation, until now the loud calls of male mammals have been shown to affect only competition between males. Although it has been suggested that loud calling could also serve to attract females, the possibility that it has a direct effect on reproduction in females has not previously been investigated for any mammal. Here I report that roaring in red deer (Cervus elaphus) advances ovulation and that harem-holding males can improve their mating success by regular calling.     

Sympatric speciation by sexual selection

There is increasing evidence for the process of sympatric speciation, in which reproductive isolation of species occurs without physical isolation. Theoretical models have focused on disruptive natural selection as the crucial pressure for splitting a species. Here we report the theoretical finding that sympatric speciation may be caused by sexual selection even without disruptive natural selection. Specifically, we show that variation in a male secondary sexual character with two conspicuous extremes and the corresponding variance in female mating preference around no preference may jointly evolve into bimodal distributions with increasing modal divergence of the male and female traits, pulling a population apart into two prezygotically isolated populations. This mode of speciation, driven by two runaway processes in different directions, is promoted by an increase in the efficiency of females in discriminating among males or a decrease in the cost of male conspicuousness, indicating that sympatric speciation may occur more readily if barrier-free or predator-free conditions arise. Although even a slight cost of female preference would cancel the runaway process of sexual selection, it would not cancel the divergent runaway processes of sympatric speciation.     

Mutation and sex in a competitive world

How do deleterious mutations interact to affect fitness? The answer to this question has substantial implications for a variety of important problems in population biology, including the evolution of sex, the rate of adaptation and the conservation of small populations. Here we analyse a mathematical model of competition for food in which deleterious mutations affect competitive ability. We show that, if individuals usually compete in small groups, then competition can easily lead to a type of genetic interaction known as synergistic epistasis. This means that a deleterious mutation is most damaging in a genome that already has many other deleterious mutations. We also show that competition in small groups can produce a large advantage for sexual populations, both in mean fitness and in ability to resist invasion by asexual lineages. One implication of our findings is that experimental efforts to demonstrate synergistic epistasis may not succeed unless the experiments are redesigned to make them much more naturalistic.     

Sex releases the speed limit on evolution

Explaining the evolutionary maintenance of sex remains a key problem in evolutionary biology. One potential benefit of sex is that it may allow a more rapid adaptive response when environmental conditions change, by increasing the efficiency with which selection can fix beneficial mutations. Here I show that sex can increase the rate of adaptation in the facultatively sexual single-celled chlorophyte Chlamydomonas reinhardtii, but that the benefits of sex depend crucially on the size of the population that is adapting: sex has a marked effect in large populations but little effect in small populations. Several mechanisms have been proposed to explain the benefits of sex in a novel environment, including stochastic effects in small populations, clonal interference and epistasis between beneficial alleles. These results indicate that clonal interference is important in this system.