Determinants of paternity success in the spider Pholcus phalangioides (Pholcidae: Araneae): the role of male and female mating behaviour

In double mating experiments, we examined whether and to what extent various male and female behavioural traits influence the course of mating and fertilization success in the cellar spider. In males, we focussed on pre-copulatory behaviour and on the rhythmic twisting movements that the male performs with his pedipalps during copulation. In females, we investigated remating decisions and the effect of female termination of copulation. Second males fertilized a high proportion of the eggs (P ₂: median 89%) despite much shorter second matings, with high variation in relative paternity success. The number of pedipalp movements (PPMs) of either male was a better predictor of paternity than copulation duration. Our results suggest that in second matings, PPMs help to remove sperm from previous males, whereas in first matings a high number of PPMs enhances fertilization success, either due to numerical sperm competition or cryptic female choice. Furthermore, we found a negative male age effect on paternity in second matings, implying that age-related deterioration of spermatozoa may promote variation in fertilization success. Female receptivity decreased significantly in second matings; only 70% of the females remated. Females that accepted a second copulation were found to terminate these much earlier and with higher probability than first matings. This suggests that the intensity of conflict between the sexes is higher in second matings. Increased intensity of sexual conflict may be responsible for stronger selection on male traits, as pre-copulatory behaviour and age only affected male copulatory performance and paternity in second matings. Electronic Publication     

Pair and extra-pair mating success relative to male quality in red-winged blackbirds

We tested whether the reproductive success of male red-winged blackbirds (Agelaius phoeniceus) varied with male secondary sexual traits or with haematozoa prevalence, and whether these patterns were consistent with females preferring genetically superior males. We also determined whether the traits that correlated with male success on their own territories were also correlated with male success at siring young on other males territories. Our analysis included data from a 6-year study involving 617 nestlings for which paternity was determined by DNA profiling. Larger males sired more young on their territories, principally because they obtained larger harems. The success of larger males at acquiring more mates did not appear to be a consequence of larger males holding larger or better-quality territories. Older and longer-lived males sired more young by extra-pair fertilizations. Larger males sired the most offspring overall (on territory + off territory). Variation in epaulet size and color, responses to male and female models, nest defence and parasitism was not correlated with male success either on or off their territories or overall. Male success in a given year was significantly correlated with success the previous year, as expected if females were selecting genetically superior males. The male that was by far the most successful individual in this study was highly consistent from year to year. Because male body size is positively correlated with survival in this population (although not within the sample of males included in this study), female preference for larger males may have reflected a general preference for males with superior Survival ability. We propose that the direct advantage realized by older males in extra-pair matings might indicate that experience is important, such that experienced males are better at creating or exploiting the opportunities for extra-pair mating. This hypothesis is consistent with a pairwise analysis of cuckoldry that showed that cuckolders were most often older than the males they cuckolded.     

Predicting the mating system from phenotypic correlations between life-history and sperm quality traits in the Alpine whitefish <Emphasis Type="Italic">Coregonus zugensis</Emphasis>

The mating behavior and reproductive strategies of Alpine whitefish like Coregonus zugensis (Nüsslin) are poorly understood, probably because they spawn in deep water where direct observations are difficult. In this study, we interpret life-history and sperm quality traits of fish that we caught from their spawning place. We found that males invest heavily into gonadal tissue (up to 5.6% of their body weight), which is, in comparison to other fish, consistent with external fertilization, distinct pairing and moderate to high communal spawning, or no pairing and low to moderate communal spawning. Sperm competition theory and recent experimental studies on other salmonids predict that males optimize ejaculate characteristics in relation to the costs of sperm and the level of competition they have to expect: dominant males are predicted to invest less into ejaculate quality and to have slower spermatozoa than subdominant males. We found that spermatozoa of older males are slower than those of younger males. Moreover, older males have larger breeding tubercles, a secondary sexual trait that has, in some previous studies, been found to be linked to good condition and to good genetic quality. Our results suggest that C. zugensis has age-linked reproductive strategies, that multimale spawning is common, i.e., that sperm competition plays a significant role, and that older males are on average dominant over younger males at the spawning place.     

Male asymmetry and postcopulatory sexual selection in the fly Dryomyza anilis

The significance of male asymmetry in postcopulatory sexual selection was studied in the fly Dryomyza anilis by examining whether male asymmetry is related to fertilization success. The traits measured were wing length, tibia length and the length of small and large claspers. The male claspers are situated at the tip of the abdomen, functional pair of claspers consists of a large and a small clasper on the same side of the body. These claspers are used to tap the female abdomen after sperm transfer, which has been shown to increase fertilization success for the mating male. Fertilization success was negatively related to the fluctuating asymmetry of wing length, suggesting either female preference for more symmetrical males or a relationship between male asymmetry and intrasexual selection which was reflected in mating performance. Fertilization success was also related to the length of small claspers, decreasing with increasing length of the claspers. In addition, males with asymmetrical small claspers enjoyed higher fertilization success than symmetrical ones. This study shows that fluctuating asymmetry in wing length is an important fitness trait in postcopulatory sexual selection. Since male tapping affects sperm distribution in the female's sperm storage organs, the higher fertilization success of males with asymmetrical small claspers could have a functional relationship with the asymmetrical position of female sperm storage organs. Received: 6 March 1997 / Accepted after revision: 8 November 1997     

Mating system and mating success of the desert spider Agelenopsis aperta

Field studies of the desert spider Agelenopsis aperta revealed a primarily monogamous mating system. However polygyny, polyandry and polygynandry were superimposed upon the primary system, with 9% of the marked males and 11% of the marked females in a field population mating more than once. In the laboratory males commonly mated multiply with fertile offspring resulting, while females were less likely than males to mate multiply. Monogamy under field conditions was enforced by two factors: (1) high travel costs to males, and (2) a significant decline in female receptivity after the first mating. Heavy males were more likely to be accepted by females both in the field, and in female choice experiments conducted in the laboratory. Finally, male weight determined the outcome of male-male agonistic interactions over females. One possible explanation for female choice in this system which lacks male parental investment is that females may be using male size as an indicator of future success of their offspring.     

Mate replacement in experimentally widowed collared flycatchers (Ficedula albicollis): determinants and outcomes

There is increasing evidence that sexual selection may be intense even in socially monogamous birds, resulting from both mate choice and sperm competition. We studied these two modes of sexual selection experimentally by removing paired male collared flycatchers, Ficedula albicollis, from their mates for 2 days and investigating the factors that influenced the likelihood of a replacement male appearing and how the removals influenced paternity. Replacement males (usually neighbouring males) appeared at 81% (n = 37) of nests where males were removed. The likelihood of this appearance was unaffected by the probable reproductive value of the female's clutch to the replacing male. A replacement was, however, less likely when the original male had a large forehead patch, a trait previously shown to be subject to sexual selection in this population. Experimental removal of males increased the level of sperm competition: 74% of experimental broods were multiply sired, compared to 29% of unmanipulated broods in a previous study. Only two factors predicted how paternity was shared between males: removed males fathered more young if removed closer to laying, and if they had larger forehead patches. The former result is consistent with last-male sperm precedence determining paternity, whereas the latter adds to other evidence that forehead patch size is the target of female preference in this species. Our results suggest that females exert some control over male replacement, and also that they may influence the fertilisation success of males by behavioural means. Received: 15 July 1998 / Received in revised form: 16 March 1999 / Accepted: 28 March 1999     

Effect of sperm depletion and starvation on female mating behavior in the water strider,Aquarius remigis

The resolution of intersexual conflict over mating should be dependent on the current state of each individual. In this study, I used a factorial design to examine the influence of two physiological factors, sperm depletion and food deprivation, on resistance to mating by females of the water strider, Aquarius remigis. Females employ several different mate-resisting tactics during an encounter with a male. Five measures of female resistance to mating were identified: jumping, rolling, dunking, time spent dunking, and struggle duration. Jump, roll, and dunk rates were highly correlated with each other and combined into one metric of resistance to mating (PC1) using principal components analysis. Time per dunk (T/D) and struggle duration were also analyzed. Discrete male behaviors during the struggle could not be identified. Two measures of female resistance, PC1 and T/D, were significantly lower in sperm-depleted females than in sperm-replenished females. Struggle duration did not differ between the two treatments. Starvation had no effect on any of the measures of resistance. Sperm depletion significantly enhanced the probability of mating (54% vs. 24% for replenished females), while starvation had no effect on the probability of mating. I pooled all the females and compared females that mated with those that did not mate. Nonmating females resisted significantly more than mating females in all three measures of resistance. Path analysis indicated that PC1 was the only measure of resistance that was significantly negatively related to the probability of mating. Almost half (46%) of sperm-depleted females showed no resistance to males, while only 3% of sperm-replenished females were nonresistant. When nonresisters were removed from the analysis, sperm depletion had no effect on any of the measures of female resistance to mating and no effect on the probability of mating. In A. remigis, female resistance appears to be a yes/no phenomenon with respect to sperm depletion and not affected directly by starvation. Received: 2 September 1994/Accepted after revision: 9 September 1995     

Fertilisation success in the fly Dryomyza anilis (Dryomyzidae): effects of male size and the mating situation

Male fertilisation success in relation to male size and the mating situation (ordinary pair formation with a single, nonvirgin female vs. take overs) was examined in the fly Dryomyza anilis. In ordinary matings, large males achieved higher fertilisation success than small ones when they were the second to mate with the female. Take overs differ from ordinary pair formation in that the second male experiences intensified sperm competition. This is because in take overs the female is not able to discharge any of the sperm inseminated by the first male as she usually does before a new mating. Compared with ordinary matings, take overs reduced the fertilisation success of the second male by 8–10%, whereas that of the first male was 7–14% higher in take overs. Even though the intruder was always larger than the paired male his superior fertilisation success did not compensate for the effect of the sperm already present in the female. In D. anilis, males can increase their fertilisation success by tapping the female's external genitalia with their claspers or having several copulation bouts per mating. Thus, in a take over, the intruder could respond to the intensified sperm competition by performing more tapping sequences per copulation bout or more copulation bouts per mating. In matings observed in the wild, males performed more tapping sequences after a take over than after pair formation with a single female, although the difference was not significant. The results show that there are differences in fertilisation success between males of different size. In addition, different mating situations can result in considerable variation in the fertilisation success of an individual male. Higher fertilisation success for the first male after a take over may be significant, in particular, for the reproductive success of small males, which frequently lose their females to large males.     

Experimental and natural changes in the peacock's (Pavo cristatus) train can affect mating success

Petrie et al. (1991) demonstrated a correlation between the degree of elaboration of peacocks' trains and their mating success, and also showed that this correlation occurred because females preferred to mate with the male that had the most elaborate train of those sampled on the lek. Although these data suggest that female choice is responsible for non-random mating in this species, they do not conclusively show that train morphology is the cue that females respond to, because they do not rule out the possible influence of another unidentified variable which is correlated with train elaboration. This paper presents an experimental test of the importance of the peacock's train in determining male mating success. If the number or arrangement of eye-spots in the peacock's train influences mating success, then changing the number of eye-spots should change mating success. This prediction was tested in an experiment where the trains of male peafowl (Pavo cristatus) were manipulated by removing a number of eye-spots between mating seasons. Peacocks with eye-spots removed showed a significant decline in mating success between seasons compared with a control group. This result, together with the observational data, supports the hypothesis that the peacock's train has evolved, at least in part, as a result of female choice.     

Male reproductive success: paternity contribution to queens and workers in Formica ants

The relative number of workers and female sexuals fathered by two males mated with a queen were directly assessed using microsatellite and allozyme markers in field colonies of the ants Formica exsecta and F. truncorum. In both species one of the two males consistently fathered more offspring than the other. There was, however, no evidence that one male might be particularly successful in fathering a disproportionally high proportion of female sexuals relative to the proportion of workers. Moreover, in F. exsecta, the proportions of worker pupae and worker adults fathered by each male did not differ significantly between cohorts. The most likely explanation for this pattern is that females store different amounts of sperm from the two males they mated with. Received: 10 January 1997 / Accepted after revision: 22 March 1997     

Sperm precedence, mating interval, and a novel mechanism of paternity bias in a beetle (Tenebrio molitor L.)

When females mate with more than one male, the ensuing sperm competition leads to the evolution of male mechanisms that skew paternity. Males of the yellow mealworm beetle (Tenebrio molitor) transfer a spermatophore to females during copulation, but sperm release and storage occur later. We investigated how the interval between two matings with different males affects sperm precedence by varying the interval between the copulations so that the second mating was either: (1) before sperm release from the first spermatophore (<5 min); (2) after sperm release but before spermatophore ejection (15–20 min); (3) after spermatophore ejection but before sperm storage (4 h), or (4) after complete sperm storage (24 h). We collected offspring over a period of 2 weeks and determined paternity by protein electrophoresis. There was second-male sperm precedence in all treatments, but when the interval was <5 min, the second male usually (86% of cases) had complete sperm precedence (i.e., P ₂=1). Investigations into the mechanism of second-male sperm precedence during <5-min mating intervals indicate that sperm release from the first spermatophore is inhibited, a phenomenon which has not been previously documented. Received: 31 January 2000 / Revised: 9 June 2000 / Accepted: 26 August 2000     

Male size and mating tactic influence proximity to females during sperm competition in bluegill sunfish

Many fishes are characterized by intense sperm competition between males that use alternative mating tactics. In externally fertilizing fishes, males’ proximity to females during spawning can be an important determinant of fertilization success. Here, we assess how mating tactic, body length, speed during streak spawns, and periphery cover affect males’ proximity to females during sperm competition in the externally fertilizing bluegill (Lepomis macrochirus). Bluegill are characterized by three mating tactics referred to as parental, sneaker, and satellite. Parentals are territorial and construct nests, while sneakers use a streaking behavior, and satellites use female mimicry to steal fertilizations from parentals. We show that a small body length is important for sneakers but not for satellites to obtain a close position to the female during spawning. Specifically, smaller sneakers obtain a closer position to females than larger sneakers in part by positioning themselves closer on the periphery of a parental’s nest before streaking but show no difference in the speed at which they streak. The amount of peripheral vegetation around a parental’s nest did not appear to affect proximity of sneakers to females, and there was no relationship between the amount of peripheral vegetation and the frequency of intrusions by either sneakers or satellites. Finally, parentals were farther from the female when a sneaker or satellite intruded than when they spawned alone with the female.     

Analysis of the causal components of assortative mating in water striders

Field studies demonstrate that natural populations of a group of water striders (Heteroptera: Gerridae) that share a common mating system are characterized by weak assortative mating by size and by large sizes of mating males and females relative to single individuals. This study presents an experimental assessment of the components of mating that may contribute to these mating patterns. The effects of male and female body size on each of three components of mating were studied in three water strider species in the laboratory. Large females of all three species mated more frequently, copulated for longer and were guarded longer than small females. Large males mated more frequently than small males in all three species, and also guarded females for longer in the two species where the average of mate guarding was long. However, we found an antagonistic effect of male size on copulation duration: small males copulated for longer than large males in all three species. We show that the combined effects of these size biases mimic the mating patterns found in the wild, e.g. weak and variable assortative mating, and stronger and less variable size ratios of mating versus non-mating females relative to males. We suggest that the antagonistic effects of male size on copulation and guarding duration may be a key source of interpopulational variation in assortative mating and sexual selection on male size. Further, neither spatial or temporal covariation in size, nor mechanical constraints, caused the assortative mating observed here in this group of water striders. Some combination of male and female choice (either active or passive forms) of large mates and male-male exploitation competition for mates play potentially important roles in producing population level assortative mating in water striders. Received: 17 March 1995/Accepted after revision: 28 October 1995     

Hermaphrodite sex role preferences: the role of partner body size, mating history and female fitness in the sea slug Chelidonura sandrana

Costs and benefits associated with matings and the effects of mating frequency on fitness commonly differ between the sexes. As a result, outcrossing simultaneous hermaphrodites may prefer to copulate in the more rewarding sex role, generating conflicts over sperm donation and sperm receipt between mates. Because recent sex role preference models remain controversial, we contrast here some of their assumptions and predictions in the sea slug Chelidonura sandrana. For this hermaphrodite with sperm storage and internal fertilisation, risk-averse models assume that fitness pay-offs are constantly higher in the female than in the male function in any single mating. Moreover, excluding mutual partner assessment, these models predict male mating behaviour to be independent of receiver traits. The competing gender ratio hypothesis assumes that relative fitness pay-offs, and thus the preferred mating roles, vary and may reverse between matings and predicts that ejaculation strategies co-vary with receiver quality. We found that field mating rates of C. sandrana substantially exceeded what is required to maintain female fertility and fecundity, indicating large variation in direct female benefits between matings. We further demonstrate that male copulation duration adaptively increased with partner body size (i.e. fecundity) but decreased with recent partner promiscuity. These findings are compatible with the gender ratio hypothesis but contradict risk-averse models.     

Fighting success and attractiveness as predictors of male mating success in the black field cricket, Teleogryllus commodus: the effectiveness of no-choice tests

Females are generally assumed to prefer larger, more dominant males. However, a growing number of studies that control for male-male competition have shown no correlation between dominance and attractiveness. Aggressive males can interfere with female mate preference either by physically coercing females into mating or by driving submissive males away and restricting mate choice. The most common method of assessing female mate choice is by using simultaneous two-choice tests. These control for male-male interactions, but usually interfere with physical and chemical cues involved in mate selection or alter male behaviour. They are therefore unsuitable for many study species, especially insects. Another method is the no-choice test that measures a females latency to mating when placed with a single male as an indication of male attractiveness. No-choice tests control for male-male aggression while allowing full contact between pairs (they allow actual mating to be directly observed rather than to occur based on a correlated behaviour). So far, however, no study has confirmed that males that entice females to mate sooner actually enjoy increased longer-term mating success. As such, the accuracy of no-choice tests as a method of examining mate choice remains untested. Here, we used no-choice tests on the black field cricket, Teleogryllus commodus, to show that (1) females did not prefer males that won fights (dominant males), and (2) latency to mating predicts actual mating success. We have clearly demonstrated the usefulness of no-choice tests and, considering the advantages of this method, they should be more often considered for a wider variety of taxa.Communicated by D. Gwynne     

Sperm traits in the quacking frog (<Emphasis Type="Italic">Crinia georgiana</Emphasis>), a species with plastic alternative mating tactics

In species where males use alternative reproductive tactics and male phenotypes are confronted with different risks of sperm competition, theory predicts that between-male-type differences in sperm expenditure may evolve. In the frog Crinia georgiana big males can monopolize females, whereas small males often engage in polyandrous matings. Consequently, big males may experience a lower risk of sperm competition than do small males. We tested if the predictions from theoretical models can be applied to the mating system of C. georgiana. Our results showed that small males do not have larger testes relative to their body size compared to their larger counterparts and that the efficiency with which sperm number, size, motility, and longevity are produced by the testes does not differ between small and large males in the predicted way. These results are not in alignment with predictions from a loaded raffle model of sperm competition on sperm expenditure in males with alternative phenotypes. The plasticity in mating tactics used by C. georgiana males and a high intraseasonal variation in male densities may have prevented the evolution of enhanced sperm performance in smaller males. A fair raffle in the sperm competition game played by C. georgiana males could also explain the observed patterns in sperm traits. Future investigations determining the parameters responsible for the deviation from theoretical predictions in this system will test the degree to which current theoretical models can indeed be applied to species with plastic reproductive tactics.     

Immune function, dominance and mating success in drumming male wolf spiders Hygrolycosa rubrofasciata

In this study, we provide a piece of experimental evidence that immune function is related to dominance and mating success in wild caught male wolf spiders, Hygrolycosa rubrofasciata. In the mating season, H. rubrofasciata males are actively searching for receptive females, and while searching males often engage in agonistic behavior (i.e., agonistic drumming signals, chases, and fights) with each other. The present results demonstrate that dominant males had higher lytic activities in their hemolymph than subordinates. Lytic activity estimates the concentration of antimicrobial peptides with lysozyme-like activity in hemolymph, which have been shown to play an important role in defense against bacteria, viruses, and fungi. Dominants also had higher courtship drumming rates than subordinates. Moreover, winners in mating competition had higher lytic activities than losers, but this was measured nonindependently of dominance status. Among males with mating failure, there was a moderate negative correlation between encapsulation rate and courtship drumming rate, suggesting that low quality males might not be able to bear the immunological costs of courtship behavior. These results suggest that females might gain immunological benefits by preferring vigorous males.     

Quantifying male attractiveness and mating behaviour through phenotypic size manipulation in the Trinidadian guppy, Poecilia reticulata

Although many studies have examined the effects of male size on attractiveness and mating behaviour, few have taken genetic background into consideration. Phenotypic manipulation permits the experimental adjustment of morphological traits while keeping genetic background constant. Here, male guppies, Poecilia reticulata, an ideal model for this type of manipulation, were raised at different temperatures to produce sibling pairs that differed in size. These were then used to investigate male mating behaviour and male attractiveness, assessed through female mate choice, in relation to this size dimorphism. Further, male–male competition, which is intrinsic to male mating behaviour, is also likely to be affected by their size. Through the use of repeated measures analyses we demonstrate that females significantly prefer larger males and male size and competition significantly affect several aspects of male mating behaviour. Larger siblings perform more sneaky mating attempts and spend more time chasing females. The frequencies of both these behaviours increase with competition. While display frequency is unaffected by male size and competition, display duration and the amount of time spent attending females are reduced in the presence of competitors. This study highlights the use of phenotypic manipulation as a valuable tool for investigating behavioural interactions and confirms that both male size and competition are significant factors in the guppy mating system.     

Proximal traits and mechanisms for biasing paternity in the red flour beetle Tribolium castaneum (Coleoptera: Tenebrionidae)

A comprehensive understanding of sexual selection requires knowledge of the traits and mechanisms responsible for increasing a male’s paternity share (proportion of progeny sired) relative to that of other males mating with the same female. In this study we manipulated by starvation the expression of traits that might influence male paternity share in Tribolium castaneum. We then conducted experiments to examine how male starvation affects male performance during sequential episodes of sexual selection from mating to progeny production, and investigated female control over specific stages by using live vs dead females. Comparison of starved vs fed males revealed that T. castaneum females have control over spermatophore transfer during mating, as live females rejected inseminations by starved (“low quality”) males. None of the measured male copulatory behaviors (leg-rubbing frequency, asymmetry, and percent of time spent rubbing) affected the probability of successful insemination, but the last two were positively associated with male paternity share. Spermatophore positioning within the female reproductive tract was not affected by male treatment (starved/fed), by female treatment (live/dead), or by male copulatory behaviors. Starvation, however, had a dramatic effect on male reproductive physiology, decreasing both accessory gland size and total number of sperms transferred (but not sperm viability in seminal vesicles). In addition, females who mated to starved males stored fewer sperms in their spermathecae, which, together with decreased ejaculate size, may explain the reduced paternity share of starved males compared to fed males. This study elucidates some cryptic mechanisms influencing male reproductive success and aids our understanding of trait evolution through sexual selection.     

Alternative reproductive tactics in male common shrews: relationships between mate-searching behaviour,sperm production,and reproductive success as revealed by DNA fingerprinting

The common shrew (Sorex araneus) is a solitary small mammal with a promiscuous mating system. Previous studies of this species suggest that females typically mate multiply, and that males may adopt alternative mate-searching tactics. We studied two generations of common shrews in a population near Oxford, England. Males were found to adopt two different mate-searching tactics. Those classed as type A occupied relatively small exclusive ranges during March, and made repeated long-distance movements to visit female ranges around the time of first oestrus in April. Males classed as type B established large overlapping ranges in areas of relatively high female density during March, and maintained these ranges throughout April. Type B males were larger than type A males at an early stage of sexual maturation, but there was no difference in the adult body size of the two types of male. Type A males had significantly higher epididymal sperm counts than type B males. Paternity analyses of litters born during the first year of the study reveal that the mean number of offspring fathered by type B males was greater than the mean number fathered by type A males. It is concluded that different mate-searching tactics may be conditional upon the timing of sexual maturation. Differences in sperm production are discussed in relation to sperm competition theory.