Inheritance Features of Mating Behavior Components in <Emphasis Type="Italic">Drosophila melanogaster</Emphasis> and Their Significance for Fitness

Components of mating behavior of Drosophila melanogaster mutant and wild-type strains were studied with respect to fitness. The magnitude of the effect of genotype on the male mating activity, female sexual receptivity, fertility and viability was determined. Strong positive correlation was found between the male mating activity and fitness components. It was shown that mating of strains contrasting in sexual behavior features can be accompanied by both heterosis and maternal effect. Inheritance coefficients were determined for sexual behavior components.__________Translated from Genetika, Vol. 41, No. 5, 2005, pp. 614–619.Original Russian Text Copyright © 2005 by Volkova, Vorobjova.     

SEXUAL SELECTION AND MALE CHARACTERISTICS IN THE BLUEHEAD WRASSE,THALASSOMA BIFASCIATUM: MATING SITE ACQUISITION,MATING SITE DEFENSE,AND FEMALE CHOICE

Through a series of replacement experiments with the bluehead wrasse, Thalassoma bifasciatum, we have identified male morphological characteristics that appear to be under phenotypic sexual selection. We were particularly interested in whether the various sources of sexual selection (male-male competition for unoccupied mating sites, defense of mating sites against small males, and female choice of males) were (1) independently associated with different phenotypic characteristics; (2) jointly affected the same characteristic in the same way; or (3) jointly affected the same characteristic in an antagonistic fashion. We replaced the resident large, brightly colored Terminal Phase (TP) males on a reef with the same number of TP males from other reefs. When transplanted, these males contest with each other to take over mating sites. The transplanted group of males were then scored for three components of fitness: (1) the quality of the site obtained through competition with other large males; (2) the male's ability to defend arriving females from small intruding males; and (3) changes in female visits to the site once the new male takes over. The first and second components are part of intrasexual selection; the third represents intersexual selection. We measured the opportunity for selection by partitioning variance in mating success, and measured the direct effects of sexual selection by estimating the covariance between morphology and fitness components. Opportunities for selection: Because females generally remain faithful to particular mating sites, most (54%) of the explainable variation in male mating success is due to the acquisition of a particular mating territory, which is the outcome of competition among TP males. There was less variation in mating success due to shifts in site use by females and defense of females against the intrusions of smaller males, but all components were significant. Effects of selection: Success in male–male competition among TP males, estimated by the quality of the territory acquired, was positively associated with body length and the relative length of the pectoral fin. Success in territorial defense against small males was primarily related to body length, with lesser contributions from body depth and the area of a white band on the flank. Contribution to fitness through female choice of males was positively associated with white band area. In the two instances where a character was associated with two fitness components, the direction of selection was the same. While body length was positively associated with winning intrasexual contests, it was not correlated to any behavioral measures of aggression. Similarly, the white band associated with attractiveness was not correlated with any aspect of courtship or aggression. Parasite load was uncorrelated with other morphological characters, and did not appear to affect any aspect of sexual selection. There was no evidence for stabilizing selection or significant additional contributions from second-order effects to the fitness surfaces. Fitness functions calculated using cubic splines were generally linear except for body length, which appeared sigmoid in its effect on site acquisition ability; this same feature tended to plateau in its effect on site defense. Analyses of the interactions of selection gradients with reef or experiment indicated that the effect of particular male characters on estimates of fitness was generally homogeneous in both time and space.     

Activity Variants of Acid Phosphatase-3 among Chromosome 3 Inversions of DROSOPHILA PSEUDOOBSCURA

Sexual selection is measured between two strains of Drosophila melanogaster: a wild strain and a strain mutant at the sepia locus. Frequency-dependent male mating was found to be successful, whereas the female genotype exerted no influence. The rarer the male genotype becomes, the greater is its mating success. A selection model is built for this behavior characteristic in which selection operates differently in the two sexes. The genetic consequencies of this model upon the maintenance of genetic polymorphism at the sepia locus are compared to experimental data from previous population cage studies. The fit obtained with this sexual selection model is compared to that of the larvel selection model previously investigated. A model composed of both sexual and larval components of fitness is presented. The role that each major selection component is expected to play in experimental populations as the gene frequency changes is discussed. Sexual selection leads to an equilibrium level higher than larval selection, and the combined model is very close to the experimental values.     

Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females

The evolution of female mate choice, broadly defined to include any female behaviour or morphology which biases matings towards certain male phenotypes, is traditionally thought to result from direct or indirect benefits which females acquire when mating with preferred males. In contrast, new models have shown that female mate choice can be generated by sexual conflict, where preferred males may cause a fitness depression in females. Several studies have shown that female Drosophila melanogaster bias matings towards large males. Here, we use male size as a proxy for male attractiveness and test how female fitness is affected by reproducing with large or small males, under two different male densities. Females housed with large males had reduced lifespan and aged at an accelerated rate compared with females housed with small males, and increased male density depressed female fitness further. These fitness differences were due to effects on several different fitness components. Female fitness covaried negatively with male courtship rate, which suggests a cost of courtship. Mating rate increased with male size, whereas female fitness peaked at an intermediate mating rate. Our results suggest that female mate choice in D. melanogaster is, at least in part, a by-product of sexual conflict over the mating rate.     

Polymorphisms in a desaturase 2 ortholog associate with cuticular hydrocarbon and male mating success variation in a natural population of Drosophila serrata

Elucidating the nature of genetic variation underlying both sexually selected traits and the fitness components of sexual selection is essential to understanding the broader consequences of sexual selection as an evolutionary process. To date, there have been relatively few attempts to connect the genetic variance in sexually selected traits with segregating DNA sequence polymorphisms. We set out to address this in a well‐characterized sexual selection system – the cuticular hydrocarbons (CHCs) of Drosophila serrata – using an indirect association study design that allowed simultaneous estimation of the genetic variance in CHCs, sexual fitness and single nucleotide polymorphism (SNP) effects in an outbred population. We cloned and sequenced an ortholog of the D. melanogaster desaturase 2 gene, previously shown to affect CHC biosynthesis in D. melanogaster, and associated 36 SNPs with minor allele frequencies > 0.02 with variance in CHCs and sexual fitness. Three SNPs had significant multivariate associations with CHC phenotype (q‐value < 0.05). At these loci, minor alleles had multivariate effects on CHCs that were weakly associated with the multivariate direction of sexual selection operating on these traits. Two of these SNPs had pleiotropic associations with male mating success, suggesting these variants may underlie responses to sexual selection due to this locus. There were 15 significant male mating success associations (q‐value < 0.1), and interestingly, we detected a nonrandom pattern in the relationship between allele frequency and direction of effect on male mating success. The minor‐frequency allele usually reduced male mating success, suggesting a positive association between male mating success and total fitness at this locus.     

Male mating success and risk of predation in a wolf spider: a balance between sexual and natural selection?

1. Traits that benefit males through sexual selection are simultaneously expected to impair males by provoking costs through natural selection. If we consider the two male fitness components, mating success and viability, then we may expect that the increase in male mating success resulting from a larger trait size will be counterbalanced by an increase in viability costs.
2. We studied the benefits and costs of male mate searching and sexual signalling activity in the wolf spider Hygrolycosa rubrofasciata . In the field, males search females actively and court them by drumming dry leaves with their abdomen. Females have been shown to prefer males with high drumming rate. Male moving and especially drumming is energetically highly demanding and drumming results in significant mortality costs.
3. Our objective in this study was to determine whether male mate-searching activity or drumming activity affect male mating success and the risk of males being predated.
4. It was evident that both higher mate-searching activity and higher drumming activity benefited males by increasing their mating success. Higher mate-searching activity clearly impaired males by causing direct increase in predation risk. There was also a slight tendency that more actively drumming males had higher risk of predation and from all of the predated males 13.3% were caught directly after they had drummed. Furthermore, male drumming activity decreased drastically in the presence of the predator.
5. We conclude that in H. rubrofasciata both increased mate-searching activity and drumming activity benefit males through sexual selection, but at the same time natural selection provokes direct balancing costs on the same traits.     

Reducing mutation load through sexual selection on males

Mutation load is a key parameter in evolutionary theories, but relatively little empirical information exists on the mutation load of populations, or the elimination of this load through selection. We manipulated the opportunity for sexual selection within a mutation accumulation divergence experiment to determine how sexual selection on males affected the accumulation of mutations contributing to sexual and nonsexual fitness. Sexual selection prevented the accumulation of mutations affecting male mating success, the target trait, as well as reducing mutation load on productivity, a nonsexual fitness component. Mutational correlations between mating success and productivity (estimated in the absence of sexual selection) were positive. Sexual selection significantly reduced these fitness component correlations. Male mating success significantly diverged between sexual selection treatments, consistent with the fixation of genetic differences. However, the rank of the treatments was not consistent across assays, indicating that the mutational effects on mating success were conditional on biotic and abiotic context. Our experiment suggests that greater insight into the genetic targets of natural and sexual selection can be gained by focusing on mutational rather than standing genetic variation, and on the behavior of trait variances rather than means.     

Cross-generational fitness benefits of mating and male seminal fluid

In many species, the physical act of mating and exposure to accessory gland proteins (Acps) in male seminal fluid reduces female survival and offspring production. It is not clear what males gain from harming their sexual partners or why females mate frequently despite being harmed. Using sterile strains of Drosophila melanogaster that differ in their production of Acps, we found that both the physical act of mating and exposure to male seminal fluid in mothers increase the fitness of daughters. We show that the changes in daughter fitness are mediated by parental effects, not by sexual selection involving good genes or owing to variation in maternal egg production. These results support the idea that male harm of females might partly evolve through cross-generational fitness benefits.     

Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components

Two factors that can affect genetic load, synergistic epistasis and sexual selection, were investigated in Drosophila melanogaster. A set of five chromosomal regions containing visible recessive mutations were put together in all combinations to create a full set of 32 homozygous lines fixed for different numbers of known mutations. Two measures of fitness were made for each line: productivity (a combined measure of fecundity and egg-to-adult survivorship) and competitive male mating success. Productivity, but not male mating success, showed a pattern of strong average synergistic epistasis, such that the log fitness declined nonlinearly with increasing numbers of mutations. Synergistic epistasis is known to reduce the mutation load. Both fitness components show some positive and some negative interactions between specific sets of mutations. Furthermore, alleles with deleterious effects on productivity tend to also diminish male mating success. Given that male mating success can affect relative fitness without changing the mean productivity of a population, these additional effects would lead to lower frequencies and lower fixation rates of deleterious alleles without higher costs to the mean fitness of the population.     

Relatively large males lower reproductive success in female zebrafish

Females can adjust their reproductive effort in relation to their partner’s perceived fitness value. In zebrafish (Danio rerio), large males are typically preferred mating partners. However, females have been observed to reduce their reproductive output with exceptionally large males but it remains unknown whether it is due to sexual harassment or aggressive behavior to establish and maintain dominance. Here, we study the association between relative male size, sexual harassment and dominance behavior, female stress status (stress behaviors and whole-body cortisol concentration), and reproductive success during a 4 day spawning trial. We found female cortisol to correlate negatively with female body size and positively with female dominance behavior. However, male and female behavior as well as female cortisol level were not related to relative male size. Females mating with relatively large males produced more and most of their eggs during the first spawning day, while females with smaller males produced few eggs during the first day but then increased egg production. Despite females produced more eggs when mating with relatively larger males, their eggs had substantially lower fertilization rates compared to females mating with relatively smaller males. Hence, overall, the reproductive fitness was lowest when females mated with a relatively large male. These findings could help to explain the maintenance of male size variation under natural conditions.     

Experimental evolution exposes female and male responses to sexual selection and conflict in Tribolium castaneum

Between-individual variance in potential reproductive rate theoretically creates a load in reproducing populations by driving sexual selection of male traits for winning competitions, and female traits for resisting the costs of multiple mating. Here, using replicated experimental evolution under divergent operational sex ratios (OSR, 9:1 or 1:6 ♀:♂) we empirically identified the parallel reproductive fitness consequences for females and males in the promiscuous flour beetle Tribolium castaneum. Our results revealed clear evidence that sexual conflict resides within the T. castaneum mating system. After 20 generations of selection, females from female-biased OSRs became vulnerable to multiple mating, and showed a steep decrease in reproductive fitness with an increasing number of control males. In contrast, females from male-biased OSRs showed no change in reproductive fitness, irrespective of male numbers. The divergence in reproductive output was not explained by variation in female mortality. Parallel assays revealed that males also responded to experimental evolution: individuals from male-biased OSRs obtained 27% greater reproductive success across 7-day competition for females with a control male rival, compared to males from the female-biased lines. Subsequent assays suggest that these differences were not due to postcopulatory sperm competitiveness, but to precopulatory/copulatory competitive male mating behavior.     

Neuropharmacological Modification of Male Sexual Behavior in Rats

We studied the dynamics of gaining sexual experience and the parameters of sexual behavior in sexually mature albino rat males subjected to pharmacological modifications of the intensity of catecholamine catabolism or the state of dopamine receptors. A monoamine oxidase inhibitor, nialamide, slowed down gaining of sexual experience and noticeably inhibited all components of the copulative act. A blocker of dopamine receptors, haloperidol, increased the variability of manifestations of the sexual activity, suppressed the motivational component of mating, but accelerated one of the components of copulative behavior (intromission). Possible mechanisms of the influence exerted by modulation of the activity of the monoaminergic systems on male sexual behavior are discussed.     

Sexual selection: harem size and the variance in male reproductive success

Sexual selection is potentially stronger than natural selection when the variance in male reproductive fitness exceeds all other components of fitness variance combined. However, measuring the variance in male reproductive fitness is difficult when nonmating males are absent, inconspicuous, or otherwise difficult to find. Omitting the nonmating males inflates estimates of average male reproductive success and diminishes the variance, leading to underestimates of the potential strength of sexual selection. We show that, in theory, the proportion of the total variance in male fitness owing to sexual selection is approximately equal to H, the mean harem size, as long as H is large and females are randomly distributed across mating males (i.e., Vharem=H). In this case, mean harem size not only provides an easy way to estimate the potential strength of sexual selection but also equals the opportunity for sexual selection, I(mates). In nature, however, females may be overdispersed with VharemH. We show that H+(k-1) is a good measure of the opportunity for sexual selection, where k is the ratio Vharem/H. A review of mating system data reveals that in nature the median ratio for Vharem/H is 1.04, but as H increases, females tend to become more aggregated across mating males with V(harem) two to three times larger than H.     

Different female mating rates in different populations do not reflect the benefits the females gain from polyandry in the adzuki bean beetle

The question why females in many species mate with several males (polyandry) has engaged the interest of evolutionary biologists for many years, and many studies have been conducted on the nature of the benefits that the females gain from polyandry. To understand the variation of female mating rates among species and populations it is indispensable to test the prediction that females of more polyandrous populations experience larger fitness benefit than those of less polyandrous populations. We compared the fitness components of two strains of the adzuki bean beetle Callosobruchus chinensis that have genetically different female mating rates. We measured the number of hatched eggs of once-copulated females and twice-copulated females in each strain. The statistical interaction for the number of hatched eggs between the number of matings and strains was determined. The increase in the number of hatched eggs is larger for the lower mating-rate strain than for the higher mating rate strain. This means that females of the lower mating-rate strain would have larger fitness gain from polyandry than those of the higher mating-rate strain. The actual mating rates of females did not reflect female interests in adzuki bean beetles, suggesting they are affected by sexual conflict.     

Lifetime Number of Mates Interacts with Female Age to Determine Reproductive Success in Female Guppies

In many species, mating with multiple males confers benefits to females, but these benefits may be offset by the direct and indirect costs associated with elevated mating frequency. Although mating frequency (number of mating events) is often positively associated with the degree of multiple mating (actual number of males mated), most studies have experimentally separated these effects when exploring their implications for female fitness. In this paper I describe an alternative approach using the guppy Poecilia reticulata, a livebearing freshwater fish in which females benefit directly and indirectly from mating with multiple males via consensual matings but incur direct and indirect costs of mating as a consequence of male sexual harassment. In the present study, females were experimentally assigned different numbers of mates throughout their lives in order to explore how elevated mating frequency and multiple mating combine to influence lifetime reproductive success (LRS) and survival (i.e. direct components of female fitness). Under this mating design, survival and LRS were not significantly affected by mating treatment, but there was a significant interaction between brood size and reproductive cycle (a correlate of female age) because females assigned to the high mating treatment produced significantly fewer offspring later in life compared to their low-mating counterparts. This negative effect of mating treatment later in life may be important in these relatively long-lived fishes, and this effect may be further exacerbated by the known cross-generational fitness costs of sexual harassment in guppies.     

Assessing the alignment of sexual and natural selection using radiomutagenized seed beetles

A major unsolved question in evolutionary biology concerns the relationship between natural and sexual selection. Sexual selection might augment natural selection, for example if mutations that harm female fecundity also reduce male mating success. Conversely, sexual selection might favour traits that impair naturally selected fitness components. We induced detrimental mutations in Callosobruchus maculatus beetles using X‐ray irradiation and then experimentally measured the effect of precopulatory sexual selection on offspring number and survival rate. Sexual selection treatment had a negative effect on egg‐to‐adult survivorship, although the number of progeny reaching adulthood was unaffected, perhaps because eggs and juveniles that failed to develop lessened competition on the survivors. We hypothesize that the negative effect of sexual selection arose because sexually competitive males transmitted a smaller nuptial gift or carried alleles that conferred reduced survival. Although we found no evidence that sexual selection on males can purge alleles that are detrimental to naturally selected fitness components, such benefits might exist in other environmental or genetic contexts.     

Effects of avian malaria on male behaviour and female visitation in lekking blue‐crowned manakins

Avian malaria, the infection by blood parasites of the genus Plasmodium, can reduce host fitness not only through mortality, but also by impairing the expression of sexual selection traits. Although different studies highlight the association of parasitism with a decrease in host reproductive success, few studies have addressed the role of parasites in honest signalling by lekking species. Hence, it is still uncertain which fitness components are affected by parasites in these species. We investigated whether avian malaria is associated with a decrease in mating behaviour of male blue‐crowned manakins Lepidothrix coronata and whether it affects female visitation in leks of a population in the central Amazon. Through behavioural observations, we estimated the rates of total male activity and social interaction, as well as the frequency of female visits at individual perches. We then examined if individuals were infected with Plasmodium spp. using molecular techniques. Avian malaria was associated with a decrease in male mating behaviour in each lek, and mating behaviour correlated with female visitation. Although rates of social interaction were not correlated with avian malaria among males, we observed that interacting with several individuals within a lek may be advantageous for males, as they also vocalized and displayed more, thus increasing their chances of being visited by females. Although female visitation was not associated with avian malaria in individuals or leks, it is still possible that female visitation is indirectly affected by avian malaria through the latter's effects on male activity. We suggest a role for male activity as an honest sexual signal for females. Thus, male display rate could be used by females as cue for the probability of a male being infected.     

Population density and group size effects on reproductive behavior in a simultaneous hermaphrodite

Background  

Despite growing evidence that population dynamic processes can have substantial effects on mating system evolution, little is known about their effect on mating rates in simultaneous hermaphrodites. According to theory, mating rate is expected to increase with mate availability because mating activity is primarily controlled by the male sexual function. A different scenario appears plausible in the hermaphroditic opisthobranch Chelidonura sandrana. Here, field mating rates are close to the female fitness optimum, suggesting that mating activity remains unresponsive to variation in mate availability.     

Why Do Female Callosobruchus maculatus Kick Their Mates?

Sexual conflict is now recognised as an important driver of sexual trait evolution. However, due to their variable outcomes and effects on other fitness components, the detection of sexual conflicts on individual traits can be complicated. This difficulty is exemplified in the beetle Callosobruchus maculatus, where longer matings increase the size of nutritious ejaculates but simultaneously reduce female future receptivity. While previous studies show that females gain direct benefits from extended mating duration, females show conspicuous copulatory kicking behaviour, apparently to dislodge mating males prematurely. We explore the potential for sexual conflict by comparing several fitness components and remating propensity in pairs of full sibling females where each female mated with a male from an unrelated pair of full sibling males. For one female, matings were terminated at the onset of kicking, whereas the other’s matings remained uninterrupted. While fecundity (number of eggs) was similar between treatments, uninterrupted matings enhanced adult offspring numbers and fractionally also longevity. However, females whose matings were interrupted at the onset of kicking exhibited an increased propensity to remate. Since polyandry can benefit female fitness in this species, we argue that kicking, rather than being maladaptive, may indicate that females prefer remating over increased ejaculate size. It may thus be difficult to assess the presence of sexual conflict over contested traits such as mating duration when females face a trade off between direct benefits gained from one mating and indirect benefits from additional matings.     

Male reproductive behavior in Drosophila melanogaster strains with different alleles of the flamenco gene

The allelic state of gene flamenco has been determined in a number of Drosophila melanogaster strains using the ovoD test. The presence of an active copy of gypsy in these strains was detected by restriction analysis. Then male reproduction behavior was studied in the strains carrying a mutation in gene flamenco. In these experiments mating success has been experimentally estimated in groups of flies. It has been demonstrated that the presence of mutant allele flamMS decreases male mating activity irrespective of the presence or absence of mutation white. The active copy of gypsy does not affect mating activity in the absence of the mutation in gene flamenco. Individual analysis has demonstrated that that mutation flamMS results in characteristic changes in courtship: flamMS males exhibit a delay in the transition from the orientation stage to the vibration stage (the so-called vibration delay). The role of locus flamenco in the formation of male mating behavior in Drosophila is discussed.