RARE MALE MATING ADVANTAGE: A REVIEW

1. The phenomenon of frequency-dependent selection with an advantage for the rare type over the common type is intriguing because it implies balancing selection. Thus the high level of genetic variability as found in natural populations can be explained without the necessity of considerable genetic load. Rare male mating advantage is here defined as frequency-dependent male sexual fitness with the rare type of male favoured. Such a rare male effect has been found to be very widespread in insects, at least under laboratory conditions, but there are several problems associated with this phenomenon which will be discussed in this review. 2. To determine whether male mating success is frequency-dependent, the quantity to be considered, most appropriately, is male sexual fitness of the one type relative to the other type (K_M). Other approaches are discussed and it is shown that they confound differential mating success with frequency dependence of mating success. Moreover, it is shown that Levene's indices, previously designed as a measure of differential mating success, confound mating success with assortment, making these indices less useful. 3. The theoretical relationship between frequency dependence of male mating success and total sexual fitness is more complicated than would be expected beforehand. Some examples are given to clarify this issue. 4. Statistical tests to determine frequency dependence of male mating success have often been carried out in the past by determining the significance of deviations from random mating for each male type frequency separately. This procedure must be considered incorrect, because a change in male mating success over frequencies has to be tested. A correct way to do this is by testing all frequencies together in one single statistic, with only a moderate assumption about the type of frequency dependence. When mating success depends on frequency in a more irregular way, alternative tests are available, in which mating success at one frequency can be tested against any other frequency. 5. The rare male effect has been studied most thoroughly in Drosophila, and has been demonstrated for many Drosophila species. The effect has been demonstrated for some other insects as well, and also for vertebrates. The rare male effect has been found for types of males differing in specific genotype (visible mutants, karyotypes), genetic background and geographic origin. A rare male effect has also been demonstrated for non-genetic properties such as temperature of rearing. Though much less common than rare male mating advantage, there are some examples of rare female mating advantage. The expression of the rare male effect may be affected by several factors, such as age of the females, temperature or experimental approach. 6. Only a few studies on rare type mating advantage in Nature have been carried out, but some positive evidence is available. 7. It is pointed out that mating success will be frequency-dependent if both types of males differ pronouncedly in mating behaviour, but the nature of this frequency dependence may vary. If one type of male is more vigorous than the other type, a one-sided rare male effect can be explained on the basis of male–male competition. Quite often, though, a two-sided rare male effect has been found for males not greatly differing in mating behaviour or mating success. Three types of explanations are considered: (a) The females prefer to choose the rare type of male; (b) The rare type of male compensates for its rarity by becoming more sexually active; (c) No individual behaviour is altered. 8. As to the question whether the rare male effect could be an artefact of the experimental setup, the following points are relevant; (a) Biases as a result of alternate marking resulting in rare male mating advantage are theoretically possible, but are shown to be unimportant in explaining the rare male effect for Drosophila. (b) An effect analogous to the effect of alternate marking due to finite sample size is conceivable, but probably less important than suggested by Bryant et al. (1980). (c) When males are not sampled randomly with respect to place in the vial, bias may be introduced, resulting in a spurious rare male effect. (d) We feel that the standpoint of Bryant et al. (1980) that there is not yet any good evidence for the existence of a rare male effect is not sustained. Positive proof in favour of the existence of the rare male effect is that the effect can be modified by changing only one factor, such as odour. The artifacts just mentioned cannot explain why a rare male effect should be present in the one but absent in the other situation.     

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.     

Insecticide resistance enhances male reproductive success in a beetle

Abstract.— Malathion-specific resistance in the red flour beetle, Tribolium castaneum , is widespread and stable in natural populations even in the absence of pesticide exposure. To understand this stability, both resistant and susceptible males were placed in competition for susceptible female fertilization. Females were then isolated and their progeny was tested for malathion susceptibility. Male reproductive success was estimated for populations originating from different geographic areas and for isogenic strains. In most cases, resistant males had a greater reproductive success rate than susceptibles. The results suggest that male reproductive success is not traded against the selection for malathion resistance, even resistant individuals are at an advantage for this fitness trait. This absence of fitness cost may be the result of postselection of (1) modifier gene which ameliorate the fitness of resistant individuals or (2) nondeleterious resistance gene. Resistant phenotype superiority could be due to increased male mating success, improved ability of resistant males in sperm competition, female mate choice, and/or cryptic female choice of resistance gene(s). The effect of male phenotypic frequency on male reproductive success was also examined. We observed that male fertilization success is frequency dependent and inversely related to their frequency. However, this "rare male" advantage did not counteract the superiority of the resistant males.     

Chemoreception, symmetry and mate choice in lizards

Research on fluctuating asymmetry (FA)-mediated sexual selection has focused almost exclusively on visual signals and ignored chemical communication despite the fact that many species rely on chemical signals for attracting mates. Female mate choice based on visual traits appears to be rare in lizards. However, the femoral glands of male lizards produce pheromones which might transmit chemical information about an individual's developmental stability. Therefore, we hypothesized that mate choice may be based on chemical cues. We analysed the effect of the developmental stability levels of males on the attractiveness of males' scents to females in a laboratory experiment with the lizard Lacerta monticola. When we offered two males of similar body size, females preferentially associated with the scents of males with low FA in their femoral pores and also with the scents of males with a higher number of femoral pores. This suggested that the females were able to discriminate the FA of the males by chemical signals alone and that the females preferred to be in areas marked by males of high quality, thus increasing their opportunities of mating with males of high quality. We suggest that the quality and/or amount of male pheromones could communicate the heritable genetic quality of a male to the female and thereby serve as the basis for adaptive female choice in lizards.     

Testing for an unusual distribution of rare variants

Technological advances make it possible to use high-throughput sequencing as a primary discovery tool of medical genetics, specifically for assaying rare variation. Still this approach faces the analytic challenge that the influence of very rare variants can only be evaluated effectively as a group. A further complication is that any given rare variant could have no effect, could increase risk, or could be protective. We propose here the C-alpha test statistic as a novel approach for testing for the presence of this mixture of effects across a set of rare variants. Unlike existing burden tests, C-alpha, by testing the variance rather than the mean, maintains consistent power when the target set contains both risk and protective variants. Through simulations and analysis of case/control data, we demonstrate good power relative to existing methods that assess the burden of rare variants in individuals.     

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.     

Female-biased dispersal and patrilocal kin groups in a mammal with resource-defence polygyny

In most mammals, dispersal rates are higher in males than in females. Using behavioural and genetic data of individually marked bats, we show that this general pattern is reversed in the greater sac-winged bat (Saccopteryx bilineata). Dispersal is significantly female biased and male philopatry in combination with rare male immigration causes a patrilineal colony structure. Female dispersal helps avoid father-daughter inbreeding, as male tenure exceeds female age at first breeding in this bat species. Furthermore, our data suggest that females may engage in extra-harem copulations to mate with genetically dissimilar males, and thus avoid their male descendants as mating partners. Acquaintance with the natal colony might facilitate territory takeover since male sac-winged bats queue for harem access. Given the virtual absence of male immigration and the possible lower reproductive success of dispersing males, we argue that enhancing the likelihood of settlement of male descendants could be adaptive despite local mate competition. We conclude that resource defence by males is important in promoting male philopatry, and argue that the potential overlap of male tenure and female first conception is the driving force for females to disperse.     

Sexually selected skin colour is heritable and related to fecundity in a non-human primate

Sexual selection promotes the prevalence of heritable traits that increase an individual''s reproductive rate. Despite theoretically strong directional selection, sexually selected traits can show inter-individual variation. Here, we investigate whether red skin ornamentation, a rare example of a male mammalian trait involved in mate attraction, influences fecundity and is heritable in rhesus macaques (Macaca mulatta), and explore the mechanisms that are involved in maintaining trait variation. Interestingly, the trait is expressed by and is attractive to both sexes. We collected facial images of 266 free-ranging individuals and modelled skin redness and darkness to rhesus macaque vision. We used 20 years of genetic parentage data to calculate selection gradients on the trait and perform heritability analyses. Results show that males who were both darkly coloured and high-ranking enjoyed higher fecundity. Female skin redness was positively linked to fecundity, although it remains unclear whether this influences male selectiveness. Heritability explained 10–15% of the variation in redness and darkness, and up to 30% for skin darkness when sexes are considered separately, suggesting sex-influenced inheritance. Our results suggest that inter-individual variation is maintained through condition-dependence, with an added effect of balancing selection on male skin darkness, providing rare evidence for a mammalian trait selected through inter-sexual selection.     

Rare HVR1-HCV genotype 1b variants in patients with B non Hodgkin's lymphoma. Comparison with viral sequences detected in cases of lymphoproliferative disorders and B cell compartmentalisation

We compared the E2-HVR1 region in HCV-1b positive B-NHL cases from a multicenter study with sequences from studies related to lymphoproliferative disorders and B cell compartmentalisation. We found rare and unique mutations both in B-NHL isolates and in cases with lymphoproliferative disorders and lymphocyte infection. These rare mutations could have an important effect on HVR1 region and, as a consequence, on the binding of E2 on CD81, with a possible implication for both antigenic stimulation and HCV entry. In conclusion, the HCV predominants circulating in B-NHL cases seem to be associated with clonal selection of rare variants.     

Role of the olfactory systems and importance of learning in the ewes' response to rams or their odors

In sheep, exposure of seasonally anestrous females to the male or its fleece results in activation of luteinizing hormone (LH) secretion and synchronized ovulation. The study of the neural pathways involved in this phenomenon, commonly named "male effect", show that the main olfactory system plays a critical role in the detection and the integration of the male odor. The accessory olfactory system participates in the perception of the ram odor but does not seem necessary for the endocrine response. According to the hypothesis that the neuroanatomical differences between the two olfactory systems could be associated with different functional roles, we investigated the importance of sexual experience and learning processes in the male effect. Our results showed that female responses depend on previous sexual experience. We also demonstrated that the LH response to male odor could result from an associative learning process. The aim of the present report was to summarize our current knowledge concerning the "male effect" and in particular to clarify the role of sexual experience and learning in the processes involved in this effect.     

Genetic analysis of a wild-caught hybrid between non-sister Heliconius butterfly species

Interspecific hybridization occurs regularly in wild Heliconius butterflies, although hybrid individuals are usually very rare. However, hybridization generally occurs only between the most closely related species. We report a rare naturally occurring hybrid between non-sister species and carry out the first genetic analysis of such distant hybridization. Mitochondrial and nuclear genes indicate that the specimen is an F1 hybrid between a female Heliconius ethilla and a male Heliconius melpomene, originating from a group of 13 species estimated to have diverged over 2.5 Myr ago. The presence of such distant natural hybrids, together with evidence for backcrossing, suggests that gene flow across species boundaries can take place long after speciation. Adaptive genes such as those involved in wing coloration could thus be widely shared among members of this highly mimetic genus.     

Demographic effects of temperature‐dependent sex determination: will tuatara survive global warming?

Global climate change is of particular concern for small and isolated populations of reptiles with temperature-dependent sex determination because low genetic variation can limit adaptive response in pivotal temperatures, leading to skewed sex ratios. We explore the demographic consequences of skewed sex ratios on the viability of a tuatara population characterized by low genetic diversity. We studied the rare species of tuatara ( Sphenodon guntheri ) on the 4 ha North Brother Island in New Zealand over two nesting seasons and captured 477 individuals, with a 60% male bias in the adult population. Females first breed at 15 years and have extremely low rates of gravidity, producing clutches of three to eight eggs every 9 years. Simulations of the population using population viability analysis showed that the current population is expected to persist for at least 2000 years at hatchling sex ratios of up to 75% male, but populations with 85% male hatchlings are expected to become extinct within approximately 300 years (some eight generations). Incorporation of inbreeding depression increased the probability of extinction under male biased sex ratios, with no simulated populations surviving at hatchling sex ratios >75% male. Because recent models have predicted that climate change could lead to the production of all male S. guntheri hatchlings by 2085, we examined whether periodic intervention to produce mixed or female biased sex ratios would allow the population to survive if only males were produced in natural nests. We show that intervention every 2–3 years could buffer the effects of climate change on population sex ratios, but translocation to cooler environs might be more cost-effective. Climate change threatens tuatara populations because neither modified nesting behaviour nor adaptive response of the pivotal temperature can modify hatchling sex ratios fast enough in species with long generation intervals.     

Female pied flycatchers trade between male quality and mating status in mate choice

According to mate choice theory, females should consider both male quality and mating status when choosing a mate. In birds, strong experimental evidence indicates that females prefer males with elaborate traits. No comparable evidence exists to determine whether females take male mating status into account or how they may trade between male quality and male mating status. We studied mate choice of female pied flycatchers (Ficedula hypoleuca) in outdoor aviaries where the effect of territory quality could be eliminated and where we could control which males were mated and which were unmated. We used male plumage colour as our measure of male quality. In the aviaries, focal females could easily compare males and assess their plumage colour and mating status, and resident females were prevented from attacking prospecting females because of separation in different compartments. The study provided evidence for a trade-off in mate choice. Females may compromise by choosing an already mated male if he is more brightly coloured and, presumably, of higher quality than available unmated males. The study did not support the idea that polygyny is based on male deception of females, but the results were consistent with the female aggression hypothesis.     

A Survey of Non-Classical Polyandry

We have identified a sample of 53 societies outside of the classical Himalayan and Marquesean area that permit polyandrous unions. Our goal is to broadly describe the demographic, social, marital, and economic characteristics of these societies and to evaluate some hypotheses of the causes of polyandry. We demonstrate that although polyandry is rare it is not as rare as commonly believed, is found worldwide, and is most common in egalitarian societies. We also argue that polyandry likely existed during early human history and should be examined from an evolutionary perspective. Our analysis reveals that it may be a predictable response to a high operational sex ratio favoring males and may also be a response to high rates of male mortality and, possibly, male absenteeism. Other factors may contribute, but our within-polyandry sample limits analysis.     

The evolution of androgenesis

It is well known that some species produce offspring carrying only female chromosomes by processes such as apomixis and parthenogenesis (generically termed "gynogenesis"). There are also several cases of natural reproduction by androgenesis in which diploid offspring carry nuclear chromosomes from only the male parent. We used population genetics models to investigate the conditions for invasion of rare androgenesis alleles and the consequences of their spread. Our models predict that androgenesis alleles often spread to fixation. If fixation causes the loss of females or female function in the population, population extinction occurs. Therefore, androgenesis alleles represent a new class of selfish genetic elements. Extinction is more likely in dioecious species than in hermaphrodites. Within dioecious species, extinction is more likely when androgenesis occurs via paternal apomixis (vs. fusion or doubling of haploid nuclei) and when females are the heterogametic sex (vs. male heterogamety). The apparent rarity of androgenesis compared to gynogenesis could be because androgenesis is harder to detect and more often leads to population extinction. Also, there could be greater evolutionary constraints on the origin of mutations for androgenesis. We suggest characteristics of groups in which further cases of androgenesis are more likely to be found.     

Consequences of lethal intragroup aggression and alpha male replacement on intergroup relations and home range use in tufted capuchin monkeys (Cebus apella nigritus)

In conflicts between primate groups, the resource-holding potential (RHP) of competitors is frequently related to group size or male group size, which can remain relatively constant for long periods of time, promoting stable intergroup dominance relationships. Demographic changes in neighboring groups, however, could introduce uncertainty into existing relationships. Among tufted capuchin monkeys (Cebus apella nigritus), dominant male replacement is a relatively infrequent demographic event that can have a profound effect on both the composition and size of the social group. Here, we report such a case and the consequences for home range use and intergroup aggression. Between June 2008 and August 2010, we periodically followed two neighboring groups (Macuco and Rita) in Iguazú National Park, recording daily paths (N = 143) and encounters between the groups (N = 28). We describe the events leading to a change in the male dominance hierarchy in the larger group (Macuco), which resulted in the death or dispersal of all adult males, followed by the succession of a young adult male to the dominant position. This takeover event reduced the numerical advantage in number of males between the two groups, although the ratio of total group sizes remained nearly constant. Following this shift in numerical asymmetry, the degree of escalation of intergroup aggression increased, and we observed reversals in the former intergroup dominance relationship. These changes in behavior during intergroup encounters were associated with changes in the use of overlapping areas. In the 6 months following the takeover, the area of home range overlap doubled, and the formerly dominant group's area of exclusive access was reduced by half. These results suggest that RHPin tufted capuchin monkeys is related to male group size. Furthermore, they highlight the importance of considering rare demographic events in attempts to understand the dynamics of aggression between primate groups.     

Sexual selection and the evolution of evolvability

Here we show that sexual selection can have an effect on the rate of mutation. We simulated the fate of a genetic modifier of the mutation rate in a sexual population with and without sexual selection (modelled using a female choice mechanism). Female choice for 'good genes' should reduce variability among male subjects, leaving insufficient differences to maintain female preferences. However, female choice can actually increase genetic variability by supporting a higher mutation rate in sexually selected traits. Increasing the mutation rate will be selected against because of the resulting decline in mean fitness. However, it also increases the probability of rare beneficial mutations arising, and mating skew caused by female preferences for male subjects carrying those beneficials with few deleterious mutations ('good genes') can lead to a mutation rate above that expected under natural selection. A choice of two male subjects was sufficient for there to be a twofold increase in the mutation rate as opposed to a decrease found under random mating.     

A male case with double aneuploidy (48,XXY,+21)

The co-occurrence of two numerical chromosomal abnormalities in same individual (double aneuploidy) is relatively rare and the clinical presentations are variable depending on the predominating aneuploidy or a combination effect of both. Furthermore, double aneuploidy involving both autosomal and sex chromosomes is seldom described. We describe a male patient with typical clinical features of Down Syndrome and his karyotype revealed 48,XXY,+21. The phenotypic characteristics of this child have been discussed in the light of the published reports on double aneuploidies of XXY and trisomy 21.     

Evolution of frequency-dependent mate choice: keeping up with fashion trends

The diversity of sexual traits favoured by females is enormous and, curiously, includes preferences for males with rare or novel phenotypes. We modelled the evolution of a preference for rarity that yielded two surprising results. First, a Fisherian 'sexy son' effect can boost female preferences to a frequency well above that predicted by mutation-selection balance, even if there are significant mortality costs for females. Preferences do not reach fixation, however, as they are subject to frequency-dependent selection: if choosy females are too common, then rare genotypes in one generation become common, and thus unattractive, in the offspring generation. Nevertheless, even at relatively low frequency, preferences maintain polymorphism in male traits. The second unexpected result is that the preferences can evolve to much higher frequencies if choice is hindered, such that females cannot always express their preferences. Our results emphasize the need to consider feedback where preferences determine the dynamics of male genotypes and vice versa. They also highlight the similarity between the arbitrariness of behavioural norms in models of social evolution with punishment (the so-called 'folk theorem') and the diversity of sexual traits that can be preferred simply because deviating from the norm produces unattractive offspring and is, in this sense, 'punished'.     

Does segregating variation in sexual or microhabitat preferences lead to non-random mating within a population of Drosophila melanogaster?

Variation in female choice for mates has implications for the maintenance of genetic variation and the evolution of male traits. Yet, estimates of population-level variation in male mating success owing to female genotype are rare. Here, we used a panel of recombinant inbred lines to estimate the strength of selection at many genetic loci in a single generation and attempt to assess differences between females with respect to the males they mated with. We performed selection assays in a complex environment to allow differences in habitat or social group preference to be expressed. We detected directional selection at loci across the genome, but are unable to provide support for differential male success because of variation in female genotype.