Theoretical aspects of sexual selection: A generalized model of mating behaviour

A model of mate selection is described in which females mate preferentially according to their probability of encounter with the males they prefer. In this model, different thresholds of response to the courtship of different male phenotypes determine the female mating preferences. Females with a lower threshold toward particular males require fewer encounters before mating with these males and more encounters before mating with any of the others. Such females mate preferentially if they encounter a male they prefer before they have been stimulated to the level of the higher threshold. At the higher threshold they mate at random. The number of the extra encounters required to raise the females' level of stimulation from the lower to the higher threshold is a parameter of the model. The frequency of the preferred males then determines the probability that a female encounters and mates with one of them before she has been sufficiently stimulated to mate at random. Sexual selection by differences in male courtship can also be described in terms of this model.The preferred characters may be determined either by dominant and recessive alleles or by each different genotype. When only one extra encounter is required before the females mate at random, the preferred males only gain a slight frequency-dependent advantage: Stable polymorphisms can only be maintained if the heterozygotes have the greater preference in their favor. When more than one extra encounter is required before random mating, the males gain a negative frequency-dependent advantage: Stable polymorphisms are generally maintained.The models are fitted to published data on the mating success of male Drosophila at varying frequencies and provide an explanation of the “rare male” effect in which less common males gain a mating advantage.     

A test for negative frequency-dependent mating success as a function of male colour pattern in the bluefin killifish

Rare male mating advantage (a form of negative frequency dependence) is frequently proposed as a mechanism for the maintenance of genetic variation within populations. This hypothesis is attractive for systems with pronounced male colour polymorphism because it can maintain particularly high levels of variation. We tested for negative frequency-dependent mating success between yellow and red male colour patterns in bluefin killifish, Lucania goodei . Lucania goodei populations harbour substantial colour pattern polymorphism, and a large proportion of this variation has a genetic basis. We established outdoor mesocosms with red and yellow males in three different ratios: yellow rare (one yellow ♂ : five red ♂), even (three yellow ♂ : three red ♂), and red rare (five yellow ♂ : one red ♂). We obtained eggs and used microsatellites to determine paternity. By contrast to expectations, we found no support for a rare male mating advantage. Red males had slightly higher spawning success than yellow males, particularly in replicates with large clutches and when red males were rare. However, yellow males did not have higher mating success when rare. We discuss alternative mechanisms for the maintenance of the polymorphism as well as the potential reasons for the lack of a rare male mating advantage.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 489–500.     

Polymorphism of melanic ladybirds maintained by frequency-dependent sexual selection

Sexual selection, whether by female preference or male competition, is almost inevitably frequency-dependent. Female preference gives rise to a 'rare male effect', by which the rarer male phenotypes gain a relatively greater selective advantage. In addition to this effect, the proportion of females expressing a preference may also be frequency-dependent.
Frequency-dependent expression of mating preference can arise in at least two ways: (1) when females encounter a succession of courting males while searching for a male they prefer; (2) when females chose a male from within a lek. Models of mating behaviour reveal a clear distinction between the frequency dependence in the expression of female preference and the frequency dependence in the consequent selection of the males. When expression of preference is highly dependent on frequency, the selection of males is constant or only slightly frequency-dependent: constant expression of preference produces high frequency dependence of selection. Analysis of general models shows that genetic polymorphisms can be maintained under a wide range of conditions.
The ladybird, Adalia bipunctata , is polymorphic for several melanic and non-melanic phenotypes. Females have a genetically determined preference for melanic males. Non-melanic phenotypes mate assortatively. By estimating the parameters of a detailed model of natural selection, sexual selection and assortative mating, it has been shown that the Adalia bipunctata polymorphism will be maintained at frequencies observed in the wild.     

Frequency dependent selection: I. Rare male phenomenon in D. subobscura dependent on the proportion of Amy genotypes and substrate composition

Analysis of the rare male mating advantage in D. subobscura, as a type of frequency dependent selection on maltose and starch media, was done by applying different statistical approaches (χ², cross-product ratio, variance and regression analysis). They reveal that mating occurs at random when proportions of prospective mates are equal, and that mating success of the males homozygous for Amy-locus genotypes (S/S and F/F) depends on their proportion. Regression analysis showed that the F/F males are sexually more active (have higher vigour) than S/S males. Rare male effect is one-sided and appears in F/F males that partake in more heterogamic matings. Comparison of the number of observed and expected homo- and heterogamic matings shows that homogamic matings are more frequent. Multifactorial analysis of variance shows that the number of matings are different for nine pairs of lines and four possible mating types (S_fS_m, S_fF_m, F_fS_m, F_fF_m). The rare male phenomenon is not dependent on different food composition, but is associated with variations in individual genotypes.     

Mechanisms for frequency-dependent mating success

We consider ways in which non-frequency-dependent processes could generate negatively frequency-dependent male mating success (the rare male effect). Various forms of male competition and female preference could produce the phenomenon, and further experiments are needed to examine their occurrence. We conclude that the rare male effect is likely to be of limited evolutionary relevance.     

Male Reproductive Success in a Promiscuous Armoured Catfish Corydoras Aeneus (Callichthyidae)

Among a variety of fish mating systems, promiscuity with random-mating seems to be most prevalent. However, detailed studies of promiscuity have been rare due partly to the peculiar difficulty in examination of male mating and reproductive success in the random mating. Females of the armoured catfish Corydoras aeneus (no sexual dimorphism other than size of males > females) spawn 10–20 egg-clutches with multiple males at a time, but an entire egg clutch is inseminated by sperm of a single male. We studied mating system of this fish in aquarium. Males had neither mating territories nor monopolized females, never being aggressive against rival males. Evidence of female preference for certain male traits including size was not detected. Females mated a male in proportion to his relative courtship frequency among males. Courtship frequency was not related to male size, and male mating success was not different between small and large males. Clutch size and insemination rate were different neither between small and large males nor between frequently and less frequently courting males. Thus, the male reproductive success will not be related to the male size, but directly to courtship frequency, indicating the random mating in this fish. There seemed to be fecundity advantage with size in female, and the consequent sexual difference in energy allocation will be responsible to the sexual dimorphism. We also discuss the low male-GSI in this promiscuous fish in which sperm competition hardly occurred.     

Rare male advantage and sex ratio

Relative success of mutant white and wild-type CS Drosophila melanogaster males is frequency-dependent, if sex ratio is 1:1. If the number of females is constant, this success depends on the ratio between the mutant and wild-type males. The sex ratio changes strongly affect the male mating activity of both genotypes.Emphasis is placed on the general interest of the Ayala equation and the Wattiaux-Lichtenberger equation in frequency-dependence and sex ratio dependence analysis.     

Social group composition modulates the role of last male sperm precedence in post-copulatory sexual selection

In many species, the order in which males mate with a female explains much of the variation in paternity arising from post-copulatory sexual selection. Research in Drosophila suggests that mating order may account for the majority of the variance in male reproductive success. However, the effects of mating order on paternity bias might not be static but could potentially vary with social or environmental factors. To test this idea, we used an existing dataset, collated from an experiment we previously published (Morimoto et al., PLoS One, 11, 2016, e0154468), with the addition of unpublished data from the same experiment. These previous experiments manipulated larval density in Drosophila melanogaster which generated variation in male and female body size, assembled groups of individuals of different sizes, and measured the mating success and paternity share of focal males. The data presented here provides information on each focal male's mating order and the frequency in which focal males remated with same females (‘repetitive matings’). We combined this information with our previously reported focal male reproductive success to partition variance in paternity into male mating order and repetitive matings across groups that differed in the body size composition of males and females. We found, as expected, that male mating order explained a considerable portion of the variance in male paternity. However, we also found that the impact of male mating order on male paternity was influenced by the body size composition of groups. Specifically, males that tended to mate last had a greater paternity advantage, and displayed lower variance, in groups containing a heterogenous mixture male body sizes than in groups with a single male body size. Repetitive mating only had a minor contribution to the variance in male paternity share across all experiments. Overall, our findings contribute to the growing body of research showing that post-copulatory sexual selection is subject to socio-ecological influences.     

Male Sexual Signals and Female Choice in Drosophila grimshawi (Diptera: Drosophilidae)

Sexual selection and sexual signaling have been prominent topics in recent behavioral studies, but limited data have led to controversy regarding these topics. For example, the Hawaiian Drosophila are often cited as examples in which female choice has resulted in the evolution of elaborate male courtship signals, but relatively few data exist to test these claims adequately. We studied D. grimshawi, a lek-forming Hawaiian Drosophila, to determine whether there was evidence for female choice without male competition and to elucidate the possible cues females use to discriminate. Male mating success was found to be nonrandom and males that courted females intensely and deposited many pheromone-containing streaks on the substrate were the most successful. Hence, multiple cues seem to be involved in male mating success in this species. Some males performed only one display, however, and may represent an alternate male mating tactic. The protein content of the adult male diet significantly influenced the level of pheromone streak deposition, and thus, foraging environment may affect the outcome of sexual selection.     

Mate Preference for Novel Phenotypes: A Fresh Face Matters

Conspicuous polymorphism in sexually selected traits is usually attributed to processes such as frequency‐dependent selection that can maintain genetic variation. Recent evidence indicates that dramatic variation of male coloration in guppies (Poecilia reticulata) is promoted by a form of frequency‐dependent selection in which males bearing rare or novel color patterns achieve higher mating success than males bearing common patterns. Active female preference for unfamiliar or rare color patterns has been implicated in generating this rare‐phenotype advantage, but the behavioral processes responsible for the preference remain unclear. To determine whether familiarity that is developed over a very short timescale can lead to a rare‐male mating advantage, we measured female response to courtship by males with color patterns that were the same as or different from that of the previous male to court. Females showed two types of short‐term preference variation in this experiment. On the first trial day, females shifted their preferences on a timescale of minutes, showing strong preference for males bearing a color pattern different from that of the immediately previous male to court. Twenty‐four hours later, females were less responsive to male courtship overall, and there was no difference in females’ response to different‐ and same‐morph males. Females also preferred males with more orange coloration on both trial days, but this color preference was independent of the preference for ‘different’ color patterns. These data suggest that the behavioral process underlying rare‐male advantage in guppies is that females prefer males bearing unfamiliar color patterns and that familiarity is determined over a very short timescale.     

Selection in natural and experimental populations of Drosophila pseudoobscura

The inverted gene arrangements of Drosophila pseudoobscura were used by Th. Dobzhansky in pioneering analyses of natural selection. Recent experiments have shed light on the mechanisms of selection contributing to the balanced polymorphism for the gene arrangements. In experimental populations, both major components of fitness, viability and fertility, are frequency dependent, and rare genotypes often have a selective advantage. Viabilities are also density dependent. The frequency dependence and density dependence of the fitness components are not universal. Some karyotypes are strongly influenced by frequency or density, some are slightly influenced, and some do not appear to be influenced at all. The role of heterozygote advantage in the selection on the gene arrangements is not clear. It is probably one important element in the overall selection, but viability and fertility do not always show a heterozygote advantage. Viability and fertility components of selection seem to be about equally important in changing inversion frequencies. Male mating success is an important component of selection in natural populations, and in one population rare male karyotypes have been found to have a pronounced mating advantage.     

Frequency dependence in matings with water-borne sperm

Negative frequency-dependent mating success--the rare male effect--is a potentially powerful evolutionary force, but disagreement exists as to whether previous work, focusing on copulating species, has robustly demonstrated this phenomenon. Noncopulating sessile organisms that release male gametes into the environment but retain their eggs for fertilization may routinely receive unequal mixtures of sperm. Although promiscuity seems unavoidable it does not follow that the resulting paternity obeys 'fair raffle' expectations. This study investigates frequency dependence in the mating of one such species, the colonial ascidian Diplosoma listerianum. In competition with an alternative sperm source males fathered more progeny if previously mated to a particular female than if no mating history existed. This suggests positive frequency-dependent selection, but may simply result from a mate order effect involving sperm storage. With fewer acclimation matings, separated by longer intervals, this pattern was not found. When, in a different experimental design, virgin females were given simultaneous mixtures of gametes at widely divergent concentrations, sperm at the lower frequency consistently achieved a greater than expected share of paternity--a rare male effect. A convincing argument as to why D. listerianum should favour rare sperm has not been identified, as sperm rarity is expected to correlate very poorly with ecological or genetic male characteristics in this pattern of mating. The existence of nongenetic female preferences at the level of colony modules, analogous in effect to fixed female preferences, is proposed. If visible to selection, indirect benefits from increasing the genetic diversity of a sibship appear the only likely explanation of the rare male effect in this system as the life history presents virtually no costs to multiple mating, and a near absence of direct (resource) benefits, whereas less controversial hypotheses of female promiscuity (e.g. trade up, genetic incompatibility) do not seem appropriate.     

The impact of Wolbachia,male age and mating history on cytoplasmic incompatibility and sperm transfer in Drosophila simulans

Most insects harbour a variety of maternally inherited endosymbionts, the most widespread being Wolbachia pipientis that commonly induce cytoplasmic incompatibility (CI) and reduced hatching success in crosses between infected males and uninfected females. High temperature and increasing male age are known to reduce the level of CI in a variety of insects. In Drosophila simulans, infected males have been shown to mate at a higher rate than uninfected males. By examining the impact of mating rate independent of age, this study investigates whether a high mating rate confers an advantage to infected males through restoring their compatibility with uninfected females over and above the effect of age. The impact of Wolbachia infection, male mating rate and age on the number of sperm transferred to females during copulation and how it relates to CI expression was also assessed. As predicted, we found that reproductive compatibility was restored faster in males that mate at higher rate than that of low mating and virgin males, and that the effect of mating history was over and above the effect of male age. Nonvirgin infected males transferred fewer sperm than uninfected males during copulation, and mating at a high rate resulted in the transfer of fewer sperm per mating irrespective of infection status. These results indicate that the advantage to infected males of mating at a high rate is through restoration of reproductive compatibility with uninfected females, whereas uninfected males appear to trade off the number of sperm transferred per mating with female encounter rate and success in sperm competition. This study highlights the importance Wolbachia may play in sexual selection by affecting male reproductive strategies.     

The complex interplay between macronutrient intake,cuticular hydrocarbon expression and mating success in male decorated crickets

The condition dependence of male sexual traits plays a central role in sexual selection theory. Relatively little, however, is known about the condition dependence of chemical signals used in mate choice and their subsequent effects on male mating success. Furthermore, few studies have isolated the specific nutrients responsible for condition‐dependent variation in male sexual traits. Here, we used nutritional geometry to determine the effect of protein (P) and carbohydrate (C) intake on male cuticular hydrocarbon (CHC) expression and mating success in male decorated crickets (Gryllodes sigillatus). We show that both traits are maximized at a moderate‐to‐high intake of nutrients in a P:C ratio of 1 : 1.5. We also show that female precopulatory mate choice exerts a complex pattern of linear and quadratic sexual selection on this condition‐dependent variation in male CHC expression. Structural equation modelling revealed that although the effect of nutrient intake on mating success is mediated through condition‐dependent CHC expression, it is not exclusively so, suggesting that other traits must also play an important role. Collectively, our results suggest that the complex interplay between nutrient intake, CHC expression and mating success plays an important role in the operation of sexual selection in G. sigillatus.     

Size and symmetry of sex combs were not related to male mating success in Drosophila melanogaster reared at different temperatures

Temperature is one of the most important climatic factors that may influence different traits (morphological, physiological or behavioral) in Drosophila. In this study, we examined the effects of two developmental temperatures (18°C and 25°C) on the size and the symmetry of sex combs (a male sexual trait) and their importance for male mating success in Drosophila melanogaster. However, the number of sex comb teeth (“size”) and its difference between right and left legs (“symmetry”) were relevant neither to male mating success nor to the growth temperatures.     

Balancing selection,sexual selection and geographic structure in MHC genes of Great Snipe

Signatures of balancing selection are often found when investigating the extremely polymorphic regions of major histocompatibility complex (MHC) genes, and it is generally accepted that selective forces maintain this polymorphism. However, the exact nature of the selection is controversial. Theoretical studies have mainly focused on overdominance and/or frequency dependent selection while laboratory studies have emphasised the role of mate choice. Empirical field data, on the other hand, have been relatively scarce. Previously we have found that geographic structure in MHC class II genes of the Great Snipe (Gallinago media) is too pronounced to be explained by neutral forces alone. Here we test the hypothesis that sexual selection on MHC alleles may be influencing this geographic structure between mountain and lowland populations. We found evidence of balancing selection acting on MHC genes in the form of a higher rate of amino-acid changing substitutions compared to silent substitutions in the peptide binding regions. Not only natural selection but also sexual selection may influence MHC polymorphism in this bird because certain MHC alleles have been found to be associated with higher male mating success. Contrary to predictions from negative frequency dependent selection, males carrying locally rare alleles did not have a mating advantage. Instead, the mating success of alleles in a mountain population was positively correlated to their relative frequency in the mountains compared to the lowlands, implying that locally adapted MHC alleles may also be favoured by sexual selection.     

Mating-induced reduction in accessory reproductive organ size in the stalk-eyed fly <Emphasis Type="Italic">Cyrtodiopsis dalmanni</Emphasis>

Background  

Internal reproductive organ size is an important determinant of male reproductive success. While the response of testis length to variation in the intensity of sperm competition is well documented across many taxa, few studies address the importance of testis size in determining other components of male reproductive success (such as mating frequency) or the significance of size variation in accessory reproductive organs. Accessory gland length, but not testis length, is both phenotypically and genetically correlated with male mating frequency in the stalk-eyed fly Cyrtodiopsis dalmanni. Here we directly manipulate male mating status to investigate the effect of copulation on the size of both the testes and the accessory glands of C. dalmanni.     

Exposure to Orange (Citrus sinensis L.) Trees, Fruit, and Oil Enhances Mating Success of Male Mediterranean Fruit Flies (Ceratitis capitata [Wiedemann])

Previous laboratory tests revealed that exposure to oranges (Citrus sinensis L.) increased the mating success of male Mediterranean fruit flies, Ceratitis capitata (Wiedemann) (medfly). This advantage may have resulted from male exposure to -copaene (a sesquiterpene hydrocarbon and known male attractant) in the peel, as pure -copaene has been shown to increase the mating success of male medflies. Working with orange trees as well, we investigated whether male exposure to nonfruiting trees, leaves (also known to contain -copaene albeit at a lower concentration than fruit), and fruit conferred a mating advantage to wild-like males in field-cage tests. Males exposed to entire nonfruiting trees or leaves had a mating advantage over control males (exposed to a nonhost plant) in trials conducted 1 day but not 3 days after exposure. Males exposed to orange fruits had higher mating success than control males (exposed to apples) in trials conducted 1 and 3 days after exposure. Enhanced mating success was observed only when males were permitted to contact the orange leaves and fruits; aroma alone did not affect male mating success. In addition, we examined whether exposure to commercially available orange oil, which also contains -copaene, enhanced the mating performance of wild-like and mass-reared sterile males. Heightened mating success was observed in trials conducted 1 and 3 days after exposure for both types of males, and in this case aroma alone had a positive effect on male mating success. Future research should attempt to identify the behavioral, physiological, or chemical mechanisms underlying the observed increases in male mating success.     

Male Mating Success and the Effect of Mating History on Ejaculate Traits in a Facultatively Parthenogenic Insect (Extatosoma tiaratum)

Males can typically increase their lifetime reproductive success by mating with multiple females. However, recent studies across a broad range of species have demonstrated physiological constraints on male multiple mating. In this study, we investigate male mating capacity in Extatosoma tiaratum, a facultative parthenogenetic phasmatid. Sperm limitation is thought to be one factor favouring the evolution and maintenance of parthenogenetic reproduction, but studies on male mating ability in facultative parthenogenetic species are extremely rare. To explore whether male mating success varies with mating history, we provided males with weekly mating opportunities with different females throughout their lives. We then observed mating success, and the variation in ejaculate size and quality within each mating. We showed that most, but not all, males can mate multiply, however the amount of ejaculate produced is variable and depends upon male body mass and mating history.     

Social isolation increases male aggression toward females in the field cricket Gryllus bimaculatus

Social isolation has often been reported to facilitate male aggressiveness in various animal species. If social isolation also escalates male aggressive behavior towards females, the mating success of the aggressive males will be low. This study evaluated the effect of social isolation on mating behavior in the field cricket Gryllus bimaculatus, which has traditionally been considered to be an asocial species. The results showed that social isolation from same-sex individuals enhanced male aggressiveness to females, and the mating success of aggressive males was reduced under the experimental conditions. More aggressive males exhibited a longer latency to court than less aggressive males. These results suggest that because male aggressiveness causes a delay in courtship, aggressive males may have reduced mating success. This demonstrated that social relationships are a critical factor affecting male mating success, even if the species is normally considered solitary.