The complexity of mating decisions in stalk‐eyed flies

All too often, studies of sexual selection focus exclusively on the responses in one sex, on single traits, typically those that are exaggerated and strongly sexually dimorphic. They ignore a range of less obvious traits and behavior, in both sexes, involved in the interactions leading to mate choice. To remedy this imbalance, we analyze a textbook example of sexual selection in the stalk‐eyed fly (Diasemopsis meigenii). We studied several traits in a novel, insightful, and efficient experimental design, examining 2,400 male–female pairs in a “round‐robin” array, where each female was tested against multiple males and vice versa. In D. meigenii, females exhibit strong mate preference for males with highly exaggerated eyespan, and so we deliberately constrained variation in male eyespan to reveal the importance of other traits. Males performing more precopulatory behavior were more likely to attempt to mate with females and be accepted by them. However, behavior was not a necessary part of courtship, as it was absent from over almost half the interactions. Males with larger reproductive organs (testes and accessory glands) did not make more mating attempts, but there was a strong tendency for females to accept mating attempts from such males. How females detect differences in male reproductive organ size remains unclear. In addition, females with larger eyespan, an indicator of size and fecundity, attracted more mating attempts from males, but this trait did not alter female acceptance. Genetic variation among males had a strong influence on male mating attempts and female acceptance, both via the traits we studied and other unmeasured attributes. These findings demonstrate the importance of assaying multiple traits in males and females, rather than focusing solely on prominent and exaggerated sexually dimorphic traits. The approach allows a more complete understanding of the complex mating decisions made by both males and females.     

Lack of species discrimination based on chemical cues by male sailfin mollies, <Emphasis Type="Italic">Poecilia latipinna</Emphasis>

When making mating decisions, individuals may rely on multiple cues from either the same or multiple sensory modalities. Although the use of visual cues in sexual selection is well studied, fewer studies have examined the role of chemical cues in mate choice. In addition, few studies have examined how visual and/or chemical cues affect male mating decisions. Male mate choice is important in systems where males must avoid mating with heterospecific females, as is found in a mating complex of Poecilia. Male sailfin mollies, Poecilia latipinna, are sexually parasitized by gynogenetic Amazon mollies, P. formosa. Little is known about the mechanism by which male sailfin mollies base their mating decisions. Here we tested the hypothesis that male sailfin mollies from an allopatric and a sympatric population with Amazon mollies use multiple cues to distinguish between conspecific and heterospecific females. We found that male sailfin mollies recognized the chemical cues of conspecific females, but we found no support for the hypothesis that chemical cues are by themselves sufficient for species discrimination. Lack of discrimination based on chemical cues alone may be due to the close evolutionary history between P. latipinna and P. formosa. Males from populations sympatric with Amazon mollies did not differentially associate with females of either of the two species when given access to both visual and chemical cues of the females, yet males from the allopatric population did associate more with conspecific females than with heterospecific females in the presence of both chemical and visual cues. The lack of discrimination by males from the sympatric population between conspecific and heterospecific females based on both chemical and visual cues suggests that these males require more complex combinations of cues to distinguish species, possibly due to the close relatedness of these species.     

Multiple male traits interact: attractive bower decorations facilitate attractive behavioural displays in satin bowerbirds

Sexually selected male courtship displays often involve multiple behavioural and physical traits, but little is known about the function of different traits in mate choice. Here, we examine female courtship behaviours to learn how male traits interact to influence female mating decisions. In satin bowerbirds (Ptilonorhynchus violaceus), successful males give highly aggressive, intense behavioural displays without startling females. Males do this by modulating their displays in response to female crouching, which signals the display intensity that females will tolerate without being startled. Females typically visit multiple males for multiple courtships before choosing a mate, and females show differing tolerance for intense displays during their first courtship with each male. We test three hypotheses that may explain this: (i) familiarity with the courting male; (ii) the order of the courtship in mate-searching; and (iii) the attractiveness of the courting male. We found that females are more tolerant of intense displays during first courtships with attractive males; this increased female tolerance may allow attractive males to give higher intensity courtship displays that further enhance their attractiveness. We then examined why this is so, finding evidence that females are less likely to be startled by males with better physical displays (bower decorations), and this reduced startling then contributes to male courtship success. This role of physical displays in facilitating behavioural displays suggests a novel mechanism by which multiple physical and behavioural traits may influence female choice.     

Multivariate quantitative genetics and the lek paradox: genetic variance in male sexually selected traits of Drosophila serrata under field conditions

Single male sexually selected traits have been found to exhibit substantial genetic variance, even though natural and sexual selection are predicted to deplete genetic variance in these traits. We tested whether genetic variance in multiple male display traits of Drosophila serrata was maintained under field conditions. A breeding design involving 300 field-reared males and their laboratory-reared offspring allowed the estimation of the genetic variance-covariance matrix for six male cuticular hydrocarbons (CHCs) under field conditions. Despite individual CHCs displaying substantial genetic variance under field conditions, the vast majority of genetic variance in CHCs was not closely associated with the direction of sexual selection measured on field phenotypes. Relative concentrations of three CHCs correlated positively with body size in the field, but not under laboratory conditions, suggesting condition-dependent expression of CHCs under field conditions. Therefore condition dependence may not maintain genetic variance in preferred combinations of male CHCs under field conditions, suggesting that the large mutational target supplied by the evolution of condition dependence may not provide a solution to the lek paradox in this species. Sustained sexual selection may be adequate to deplete genetic variance in the direction of selection, perhaps as a consequence of the low rate of favorable mutations expected in multiple trait systems.     

Differential rates of phenotypic introgression are associated with male behavioral responses to multiple signals

Sexual selection on multiple signals may lead to differential rates of signal introgression across hybrid zones if some signals contribute to reproductive isolation but others facilitate gene flow. Competition among males is one powerful form of sexual selection, but male behavioral responses to multiple traits have not been considered in a system where traits have introgressed differentially. Using playbacks, mounts, and a reciprocal experimental design, we tested the hypothesis that male responses to song and plumage in two subspecies of red‐backed fairy‐wren (Malurus melanocephalus) explain patterns of differential signal introgression (song has not introgressed, whereas plumage color has introgressed asymmetrically). We found that males of both subspecies discriminated symmetrically between subspecies’ songs at a long range, but at a close range, we found that aggression was equal for both subspecies’ plumage and songs. Taken together, our results suggest that male behavioral responses hinder the introgression of song, but allow for the observed asymmetrical introgression of plumage. Our results highlight how behavioral responses are a key component of signal evolution when recently divergent taxa come together, and how differential responses to multiple signals may lead to differential signal introgression and novel trait combinations.     

Exploring the influence of individual courtship behaviors on male mating success in a blow fly

Male courtship behavior and displays influence female mating decisions, and therefore affect mating success in a diverse range of organisms. While there is substantial evidence confirming that females prefer males who invest more in courtship, less attention has been paid to the relative importance of individual behaviors, and the discrete sequences of courtship that result in mating success. The small hairy maggot blow fly, Chrysomya varipes, performs stereotyped courtship behaviors, involving orienting, tapping, waving, arching, wing vibration and mounting. This study aimed to quantify male investment in specific courtship behaviors, and compare courtship investment and behavioral transitions between males who gained mating success (successful males) and those that did not (unsuccessful males). Our results show that mating success was influenced by the behaviors orienting, tapping, arching and mounting. Behavioral transitions revealed a distinct pattern of behaviors leading to a mating attempt, and some differences were observed between successful and unsuccessful males. Overall, our findings suggest that female mating decisions were based on differences in specific male courtship behaviors. This detailed observational study has quantified multiple courtship behaviors for the first time in C. varipes, and highlights the importance of considering multiple behavioral traits when exploring the influence of male courtship on mating success.     

Relationships among male sexually selected traits in the bean bug,Riptortus pedestris (Heteroptera: Alydidae)

Current concepts of sexual selection suggest that male reproductive success is determined by multiple sexual traits. As expression and production of multiple sexual traits are frequently associated with each other, positive or negative correlations among multiple sexual traits ensue. These relationships among traits associated with male reproductive success may be crucial in the evolution of male reproductive strategies. Here, we investigate phenotypic relationships among sexually selected traits in the armed bean bug Riptortus pedestris. In this insect, males with a larger body and weapon are more likely to win male–male competitions, and males with a larger weapon or higher courtship rate are more attractive to females. There was a significant positive correlation between body size and weapon size, whereas the courtship rate had significant negative correlations with body size and weapon size. Our results suggested that there was a phenotypic trade‐off between courtship rate and male morphology. In this insect, smaller males may make more effort in courtship behavior as an alternative mating tactic.     

Acoustic preference functions and sexual selection on the male calling song in the grasshopper Chorthippus biguttulus

Male courtship songs have two functions in species recognition and intraspecific mate choice. Female preference might thus exert different types of selection pressure on male song traits. We used a combination of acoustic mate choice experiments and statistical analyses to examine how traits of the calling songs of male nightingale grasshoppers,Chorthippus biguttulus , are influenced by different sexual selection pressures. We recorded calling songs of males and tested their attractiveness to females in acoustic mate choice experiments. The attractiveness values were a good estimate of the potential male mating success. In experiments with a pair of males, females copulated significantly more often with the male that had the higher attractiveness value. To detect directional, stabilizing, disruptive or correlative selection acting on male song properties we used linear and nonlinear regressions between male song traits and female response behaviour. Three signal traits were revealed to be under directional selection: song loudness, pause to syllable ratio and the mean duration of gaps within syllables. A nonlinear regression testing for correlative selection showed that a fourth song trait, rhythm, in combination with mean gap duration was also important for female mate choice. With these traits and trait combinations we were able to explain 42% of the variance in attractiveness between males. Since we found no evidence for stabilizing selection, but ample evidence for directional selection, we conclude that selection on the traits examined is related to mate choice mainly in the context of intraspecific sexual selection and probably less so in species recognition. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

The multiple signals assessed by female satin bowerbirds: could they be used to narrow down females' choices of mates?

Female choice based on multiple male traits has been documented in many species but the functions of such multiple traits are still under debate. The satin bowerbird has a polygynous mating system in which males attract females to bowers for mating; females choose mates based on multiple aspects of males and their bowers. In this paper, we demonstrate that females use some cues to decide which males to examine closely and other cues to decide which males to mate with. Female visitation rates to bowers were significantly related to male size and the males' 'solitary' display rates, and, to a lesser extent, to the numbers of bower decorations. After controlling for female visitation rates, it was found that a male's mating success was significantly related to his size and the rate at which he 'painted' his bower with saliva and chewed up plant material.     

Mate choice decision rules: Trait synergisms and preference shifts

An important and understudied question in sexual selection is how females evaluate information from multiple secondary sexual traits (SSTs), particularly when expression of traits is phenotypically uncorrelated. We performed mate choice experiments on zebra finches (Taeniopygia guttata castanotis Gould) to evaluate two hypotheses: preference shifts (obstacles to choice using one trait increase chooser reliance on others) and trait synergisms (choice based on the sum/product of two or more independently varying traits). The first experiment, which employed males raised on diets that impact SST expression, supported the trait synergism hypothesis: overall, male pairing success was best predicted by synergisms involving beak color and cheek patch size. Results did not support the preference shift hypothesis. Results of a follow‐up experiment that included males reared on a single diet, and in which male beak color and cheek patch size were manipulated, were also consistent with the trait synergism hypothesis. Results have implications for understanding the long‐term persistence of multiple SSTs in populations and for the measurement of repeatability and heritability of mate preferences.     

Sperm influences female hibernation success, survival and fitness in the bumble-bee Bombus terrestris

We present evidence that in the absence of the transfer of male gland compounds in the ejaculate as well as of behavioural male traits, such as mate guarding or harming of females, sperm itself affects female life-history traits such as hibernation success, female longevity and female fitness. Using the bumble-bee Bombus terrestris, we artificially inseminated queens (females) with sperm from one or several males and show that sire groups (groups of brother males) vary in their effects on queen hibernation survival, longevity and fitness. In addition, multiply inseminated queens always had a lower performance as compared to singly inseminated queens. Apart from these main effects, sire groups (in situations of multiple insemination) affected queen longevity and fitness not independently of each other, i.e. certain sire group combinations were more harmful to queens than others. So far, the cause(s) of these effects remain(s) elusive. Harmful male traits as detected here are not necessarily expected to evolve in social insects because males depend on females for a successful completion of a colony cycle and thus have strong convergent interests with their mates.     

Tradeoffs limit the evolution of male traits that are attractive to females

Tradeoffs occur between a variety of traits in a diversity of organisms, and these tradeoffs can have major effects on ecological and evolutionary processes. Far less is known, however, about tradeoffs between male traits that affect mate attraction than about tradeoffs between other types of traits. Previous results indicate that females of the variable field cricket, Gryllus lineaticeps, prefer male songs with higher chirp rates and longer chirp durations. In the current study, we tested the hypothesis that a tradeoff between these traits affects the evolution of male song. The two traits were negatively correlated among full-sibling families, consistent with a genetically based tradeoff, and the tradeoff was stronger when nutrients were limiting. In addition, for males from 12 populations reared in a common environment, the traits were negatively correlated within populations, the strength of the tradeoff was largely invariant across populations, and the within-population tradeoff predicted how the traits have evolved among populations. A widespread tradeoff thus affects male trait evolution. Finally, for males from four populations assayed in the field, the traits were negatively correlated within and among populations. The tradeoff is thus robust to the presence of environmental factors that might mask its effects. Together, our results indicate there is a fundamental tradeoff between male traits that: (i) limits the ability of males to produce multiple attractive traits; (ii) limits how male traits evolve; and (iii) might favour plasticity in female mating preferences.     

The evolution of female mating preferences: differentiation from species with promiscuous males can promote speciation

Females of many species are frequently courted by promiscuous males of their own and other closely related species. Such mating interactions may impose strong selection on female mating preferences to favor trait values in conspecific males that allow females to discriminate them from their heterospecific rivals. We explore the consequences of such selection in models of the evolution of female mating preferences when females must interact with heterospecific males from which they are completely postreproductively isolated. Specifically, we allow the values of both the most preferred male trait and the tolerance of females for males that deviate from this most preferred trait to evolve. Also, we consider situations in which females base their mating decisions on multiple male traits and must interact with males of multiple species. Females will rapidly differentiate in preference when they sometimes mistake heterospecific males for suitable mates, and the differentiation of female preference will select for conspecific male traits to differentiate as well. In most circumstances, this differentiation continues indefinitely, but slows substantially once females are differentiated enough to make mistakes rare. Populations of females with broader preference functions (i.e., broader tolerance for males with trait values that deviate from females' most preferred values) will evolve further to differentiate if the shape of the function cannot evolve. Also, the magnitude of separation that evolves is larger and achieved faster when conspecific males have lower relative abundance. The direction of differentiation is also very sensitive to initial conditions if females base their mate choices on multiple male traits. We discuss how these selection pressures on female mate choice may lead to speciation by generating differentiation among populations of a progenitor species that experiences different assemblages of heterospecifics. Opportunities for differentiation increase as the number of traits involved in mate choice increase and as the number of species involved increases. We suggest that this mode of speciation may have been particularly prevalent in response to the cycles of climatic change throughout the Quaternary that forced the assembly and disassembly of entire communities on a continentwide basis.     

Exploring the relationship between parental relatedness and male reproductive success in the Antarctic fur seal Arctocephalus gazella

Recent genetic studies of natural populations have shown that heterozygosity and other genetic estimates of parental relatedness correlate with a wide variety of fitness traits, from juvenile survival and parasite resistance to male reproductive success. Many of these traits involve health and survival, where the underlying mechanism may involve changes in the effectiveness of the immune system. However, for traits such as reproductive success, the likely mechanisms remain less obvious. In this paper, we examine the relationship between heterozygosity and a range of traits that contribute to male reproductive success, including time spent on territories and competitiveness. Our analysis is based on observational and genetic data from eight consecutive breeding seasons at a colony of the Antarctic fur seal, Arctocephalus gazella. Overall, male reproductive success was found to correlate strongly with internal relatedness (IR, a form of heterozygosity). When different components of success were analyzed, we found that IR correlates independently with reproductive longevity, time spent ashore, and competitive ability per unit mating opportunity on the study beach, with more heterozygous males being more successful. Behavioral observations were sufficiently detailed to allow examination of how daily mean IR values for males present on the beach varied within seasons and from year to year. Again, significant variation was found both among and within seasons, with more homozygous males appearing less able to hold territories in poor seasons when pup production is low and, within a season, at both the start of the season and to some extent around the peak of female estrus. Finally, we tested whether the benefits of high heterozygosity are due mainly to a genomewide effect (e.g. inbreeding depression) or to single locus heterosis by asking whether the relationship between IR and male success was robust to the removal of any single locus or to any pair of loci. Since the relationship remained significant in all cases, we favor a multilocus explanation for the effects we report.     

Intraspecific variation in ejaculate traits of the northern watersnake (Nerodia sipedon)

Sperm competition occurs when the sperm of more than one male compete to fertilize the eggs of a female. In reptiles, sperm competition is particularly prevalent and is an important agent of sexual selection in males. Spermatogenesis in reptiles can be energetically expensive, suggesting that there may be costs to producing high-quality ejaculates. The northern watersnake Nerodia sipedon has a mating system characterized by aggregations in which a single female mates with multiple males, resulting in high levels of multiple paternities. Under these circumstances sperm competition is likely important, and selection should favour sperm and ejaculate traits that enhance a male's reproductive success. In this study, we examined intraspecific variation in ejaculate quality (sperm length, motility, sperm density, spermactocrit) in male watersnakes and determined whether ejaculate traits varied with body size and condition, using both size-corrected mass and haematocrit as indices of condition. We found large variation among males in all these traits, except for sperm length. Although there was significant variation in sperm length among males, the majority of variation in sperm length occurred within rather than among individuals. Males with high haematocrit had sperm that were less variable with respect to length, and large males produced ejaculates that were less concentrated with respect to sperm than small males. The lack of condition dependence of most ejaculate traits is consistent with previous studies that indicate that male reproductive effort in this species is generally not energy limited, perhaps because of opportunistic foraging during the mating season.     

Me against who? Male guppies adjust mating behaviour according to their rival’s presence and attractiveness

Sexual selection theory suggests that males need to constantly reappraise their mating decisions to take account of the presence and the phenotypes of their rivals. Here we examine this expectation by asking: (i) If the presence of a rival influences male mating behaviour; (ii) How important is the attractiveness of the rival (absolute attractiveness) in shaping male behaviour; and (iii) How does a male's attractiveness in comparison to his rival (relative attractiveness) influence a male's mating decisions. Using the Trinidadian guppy, a species in which female mate choice (based on males’ attractive traits) plays an important role in male mating outcomes, we recorded the frequency of courtship displays and unsolicited attempts by focal males. First, we quantified focal male mating behaviour with and without a rival. Since the probability of a successful mating is, on average, halved by the presence of a rival, we predicted that under competition the focal male would invest more in less costly mating tactic—unsolicited attempts. Second, we examined how the rival's standard length and area of orange coloration mediated focal male mating behaviour. We found that rival presence influenced how focal males responded to females in terms of both mating tactics. However, the rival attractiveness elicited changes only in male courtship display. Focal males increased courtship display rate if his rival was small or if possessed large amounts of orange, regardless of considering rival absolute or relative attractiveness. Our results show that males invest in the costlier mating tactic when there is no rival or in the presence of a smaller rival. Interestingly, they make a similar investment in the presence of an attractive orange rival. Overall, this study highlights the importance of fine‐grained male decisions in mating encounters and shows that mating tactics are differentially shaped by multiple competition risk cues.     

A test of the Darwin–Fisher theory for the evolution of male secondary sexual traits in monogamous birds

The Darwin–Fisher theory proposes that the presence of male secondary sexual traits in monogamous birds is selected for by early season breeding of females that are in good condition. These early breeding females have high fecundity because of their good condition, and they select mates based on secondary sex traits. We tested whether this hypothesis may be responsible for the presence of male sexual ornaments in the great frigatebird, a socially and genetically monogamous seabird. Consistent with the Darwin–Fisher theory, we found that reproductive success declined over the season. However, males with more exaggerated ornaments were not chosen as mates earlier in the season than males with less exaggerated ornaments, and selection gradients on these ornaments were not significantly different from zero.     

Male reproductive fitness and queen polyandry are linked to variation in the supergene Gp-9 in the fire ant Solenopsis invicta

Supergenes are clusters of tightly linked loci maintained in specific allelic combinations to facilitate co-segregation of genes governing adaptive phenotypes. In species where strong selection potentially operates at different levels (e.g. eusocial Hymenoptera), positive selection acting within a population to maintain specific allelic combinations in supergenes may have unexpected consequences for some individuals, including the preservation of disadvantageous traits. The nuclear gene Gp-9 in the invasive fire ant Solenopsis invicta is part of a non-recombining, polymorphic supergene region associated with polymorphism in social organization as well as traits affecting physiology, fecundity and behaviour. We show that both male reproductive success and facultative polyandry in queens have a simple genetic basis and are dependent on male Gp-9 genotype. Gp-9(b) males are unable to maintain exclusive reproductive control over their mates such that queens mated to Gp-9(b) males remain highly receptive to remating. Queens mated to multiple Gp-9(B) males are rare. This difference appears to be independent of mating plug production in fertile males of each Gp-9 genotype. However, Gp-9(b) males have significantly lower sperm counts than Gp-9(B) males, which could be a cue to females to seek additional mates. Despite the reduced fitness of Gp-9(b) males, polygyne worker-induced selective mortality of sexuals lacking b-like alleles coupled with the overall success of the polygyne social form act to maintain the Gp-9(b) allele within nature. Our findings highlight how strong worker-induced selection acting to maintain the Gp-9(b) allele in the polygyne social form may simultaneously result in reduced reproductive fitness for individual sexual offspring.     

Selection of male traits during and after copulation in the seedbug Lygaeus simulans (Heteroptera, Lygaeidae)

In order to evaluate selection of male morphological traits during copulation, a laboratory experiment was performed with the promiscuous seedbug Lygaeus simulans. Three male traits suspected as putative targets of selection were measured: weight, fluctuating asymmetry of a measure on the forewings, and length of a conspicuous genital structure, the processus gonopori. As fitness measures we considered total fecundity (number of fertilized eggs), insemination and fertilization success (established if a female laid fertilized eggs after copulation), and the interval between copulation and oviposition. Eighty-four males were allowed a single copulation with one virgin female each. Out of 67 copulations, 27 (40.2%) resulted in fertilized eggs and the oviposition latency ranged from 6 to 26 days. Regressions of male traits on the fitness measures showed significant phenotypical selection of two male traits: (1) males of average weight are more likely to achieve fertilization and (2) the oviposition latency was shorter for males with lower asymmetry. The copulation-oviposition interval may be especially important for male fertilization success because Lygaeus males perform copulatory mate guarding and the last male copulating with a female fertilizes most of the eggs. No selection of the genitalic trait was detected.     

The relative importance of different direct benefits in the mate choices of a field cricket

Discussions about the evolution of female mating preferences have often suggested that females should express multiple strong preferences when different male traits are correlated with different mating benefits, yet few studies have directly tested this hypothesis by comparing the strength of female preferences for male traits known to be correlated with different benefits. In the variable field cricket, Gryllus lineaticeps, females receive fecundity and fertility benefits from mating with males with higher chirp rates and life-span benefits from mating with males with longer chirp durations. Although females prefer higher chirp rates and longer chirp durations when the other trait is held constant, it is possible that they give priority to one of these song traits when both vary. In this study, we examined the relative importance of chirp rate and chirp duration in female mate choice using single-stimulus presentations of songs that varied in both chirp rate and chirp duration. Females expressed both directional and stabilizing preferences based on chirp rate, responding most strongly to a chirp rate approximately one standard deviation above the population mean. Females did not express preferences based on chirp duration, and did not express correlational preferences. These results suggest that females may give priority to the reproductive benefits provided by males that produce higher chirp rates.