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.     

The cost of mating with a non-virgin male in a monandrous butterfly: experimental evidence from the speckled wood, Pararge aegeria

Contrary to vertebrates, sperm production in insects may bear considerable costs for males. This is especially true in species that donate spermatophores containing sperm and nutrient-rich accessory gland products like in butterflies. Hence, spermatophores at first and subsequent copulations can differ in a quantitative and qualitative way. Such effects have particularly been shown in polyandrous species providing large spermatophores. Here we experimentally tested the effect of male mating status (virgin male vs recently mated male) on copulation duration, spermatophore size and females’ fitness components in a monandrous butterfly Pararge aegeria that typically donates small spermatophores. Copulations with non-virgin males lasted on average five times longer than that with virgin males and resulted in a spermatophore which was on average three times smaller. Number of eggs laid and female life span were not affected by the mating status treatment, but there was a significant effect on the number of living caterpillars a female produced, as copulations with virgin males resulted in higher numbers of larval offspring. Interestingly, the difference in spermatophore mass at the first and the second copulation increased with male body size. This suggests differential spermatophore allocation decisions among males of different size. Consequences for females and potential mechanisms influencing female fitness components are discussed. Given the small absolute size of spermatophores in P. aegeria, components other than consumable nutrients (perhaps hormones) should cause the observed effects.     

Does male harassment of females contribute to reproductive synchrony in the grey seal by affecting maternal performance?

We investigated the possibility that male harassment of lactating females differed in relation to time of birth in the grey seal, Halichoerus grypus, on Sable Island, Nova Scotia. This was done by comparing the frequency of male disturbances, maternal performance and pup growth for females that either gave birth during the peak of the pupping season or after the peak. Of the females, 58% gave birth in a 7-day period near the beginning of the pupping period, when the operational sex ratio was 2–4 females per male. Late in the pupping period the operational sex ratio reversed to about 1 female for every 2 males. The relative frequency of disturbances by males was significantly greater for late-pupping mothers than for peak-pupping ones (1.9 vs. 1.4 encounters/h). Females that gave birth late also were disturbed by males 3 times more often than females that gave birth during the peak (3.4 vs. 1.1 % of observation time). Late-pupping mothers spent 22% less time suckling (4.0 vs. 5.1 % of observation time), had 30% slower growing pups (1.7 vs. 2.4 kg/d), and weaned pups that were 16% lighter (45.6 vs. 54.0 kg). The effect of birth time on pup mass gain and weaning mass was not attributable to factors such as maternal mass, pup birth mass or pup sex. We conclude that the reduced maternal performance is likely the result of the increased male harassment. As reduced weaning mass can lead to reduced juvenile survival, male harassment may have contributed to the enhanced reproductive synchrony in this species.     

The cost of success: reproductive effort in male southern elephant seals (<Emphasis Type="Italic">Mirounga leonina</Emphasis>)

Reproductive effort is a key parameter of life history because it measures the resources allocated to reproduction at the expense of growth and maintenance. Male reproductive effort always had a minor role with respect to female effort both in the development of theories and in field research. Elephant seals are an ideal subject for reproductive effort studies because they fast during the breeding season, splitting the phase of energy acquisition from the phase of energy use for breeding. In this paper, we present results on male reproductive effort (weight loss estimated by photogrammetry) in southern elephant seals (Mirounga leonina), the most dimorphic and polygynous of all mammal species. We show that total reproductive effort increases with age, with no sign of late decrease or senescence. Male reproductive effort in this species depends mostly on behavioral factors, i.e., the success in competition with other males, and the intensity of interaction with females. A large effort results in large gains in both mating success and fertilizations. The large reproductive success that a few males are able to achieve come at a big cost in terms of energy expenditure, but this cost does not seem to affect the likelihood of survival to the following breeding season.     

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.     

Female reactions to male absence after pairing in the pied flycatcher

Mating with an already mated pied flycatcher (Ficedula hypoleuca) male is costly for a female. Two hypotheses explain why some females still mate with already mated males. The deception hypothesis suggests that some females mate with already mated males since it is difficult to assess perfectly the mating status of a male with separate territories (polyterritoriality). The search cost hypothesis states that females are aware of male mating status but the costs of searching for an unmated male exceed costs associated with the status of secondary female. One potential cue that could disclose a male's mating status is the existence of brief visits to the primary territory by polyterritorial males. To mimic such visits I removed the male from the territory for 60 min soon after female settlement. Only few females abandoned their mates as a consequence of male removal even though they had available unmated males close by. This result is most consistent with the deception hypothesis. Females did not use occasional male absence as a cue to avoid presumably polyterritorial males and in this respect they were not perfect in assessing males.     

Testosterone-induced depression of male parental behavior in the barn swallow: female compensation and effects on seasonal fitness

In birds, many aspects of male socio-sexual and parental behavior are influenced by androgens, most notably testosterone (T). We report the effects of subcutaneous T-implants in male barn swallows (Hirundo rustica) on male and female parental behavior and on seasonal reproductive success. Males were assigned to one of three experimental groups: (i) implanted with a T-filled Silastic tube; (ii) implanted with an empty Silastic tube; and (iii) not implanted. T-implanted males provided a smaller proportion of feedings (number of feedings by the male/total number of feedings by both parents) and fed nestlings less frequently (number of feedings/h) than males of the other two groups. Females paired to T-implanted males fed nestlings significantly more often than females paired with unimplanted males. Females almost fully compensated for their mates' shortfall, and this resulted in similar combined feeding efforts among treatments. Reproductive success in their first broods or during the entire breeding season was unaffected by T- treatment. These results confirm earlier reports of the suppressive effects of T on male parental behavior. However, they are inconsistent with current ESS models that predict partial compensation as the optimal response by one individual to reduction of parental effort by its mate in monogamous, biparental systems.     

Offensive and defensive sperm competition roles in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae)

Sperm competition is predicted to generate opposing selection pressures on males. On one hand, selection should favour ‘defensive’ adaptations that protect a male’s ejaculate from displacement, while, on the other hand, selection should favour ‘offensive’ adaptations that overcome paternity assurance mechanisms of rivals. Here, we use the sterile male technique to assess sperm precedence when a male dung beetle Onthophagus taurus mates in both a defensive (first male) and an offensive (second male) role. Significant variation in a male’s sperm precedence (both P ₁ and P ₂) was detected, and an individual’s defensive (P ₁) and offensive (P ₂) abilities were positively correlated. Thus, it appears that sexual selection simultaneously selects for ‘defensive’ and ‘offensive’ adaptations in O. taurus. We discuss a variety of male traits in O. taurus that potentially contribute to a male’s ability to be successful when mating in an ‘offensive’ and a ‘defensive’ role.     

Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)—male monopolisation, female mate choice or post-copulatory mechanisms?

One of the basic principles of sexual selection is that male reproductive success should be skewed towards strong males in species with anisogamous sex. Studies on primate multi-male groups, however, suggest that other factors than male fighting ability might also affect male reproductive success. The proximate mechanisms leading to paternity in multi-male primate groups still remain largely unknown since in most primate studies mating rather than reproductive success is measured. Furthermore, little research focuses on a female’s fertile phase. The aim of this study was to investigate the relative importance of male monopolisation and female direct mate choice for paternity determination. We also investigated the extent to which paternity was decided post-copulatory, i.e. within the female reproductive tract. We used a combined approach of behavioural observations with faecal hormone and genetic analysis for assessment of female cycle stage and paternity, respectively. The study was carried out on a group of wild long-tailed macaques living around the Ketambe Research Station, Gunung Leuser National Park, Indonesia. Our results suggest that both male monopolisation and post-copulatory mechanisms are the main determinants of male reproductive success, whereas female direct mate choice and alternative male reproductive strategies appear to be of little importance in this respect. Female cooperation may, however, have facilitated male monopolisation. Since paternity was restricted to alpha and beta males even when females mated with several males during the fertile phase, it seems that not only male monopolisation but also post-copulatory mechanisms may operate in favour of high-ranking males in long-tailed macaques, thus reinforcing the reproductive skew in this species.     

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     

Seminal fluid protein depletion and replenishment in the fruit fly, <Emphasis Type="Italic">Drosophila melanogaster</Emphasis>: an ELISA-based method for tracking individual ejaculates

In many species, seminal fluid proteins (SFPs) affect female post-mating behavioral patterns, including sperm storage, egg laying, feeding, and remating. Yet, few studies have investigated the patterns of allocation, depletion, and replenishment of SFPs in male animals, despite the importance of these proteins to male and female reproductive success. To investigate such SFP dynamics, it is necessary to have a sensitive method for quantifying SFP levels in males and mated females. We developed such a method by adapting the enzyme-linked immunosorbent assay (ELISA) using anti-SFP antibodies. Here, we first use two Drosophila melanogaster SFPs (ovulin and sex peptide) to demonstrate that ELISAs provide accurate measures of SFP levels. We find that, consistent with previous data from Western blotting or immunofluorescence studies, levels of both ovulin and sex peptide decline in the mated female with time since mating, but they do so at different rates. We then use ELISAs to show that males become depleted of SFPs with repeated matings, but that previously mated males are able to transfer “virgin” levels of SFPs after 3 days of sexual inactivity. Finally, we demonstrate that ELISAs can detect SFPs from wild-caught D. melanogaster males and, thus, potentially can be used to track mating patterns in the wild. This method of measuring SFP dynamics can be used in a wide range of species to address questions related to male reproductive investment, female mating history, and variation in female post-mating behavioral changes. Norene A. Buehner and Anthony C. Fiumera contributed equally to this work.     

Mating system of a Neotropical roost-making bat: the white-throated, round-eared bat, Lophostoma silvicolum (Chiroptera: Phyllostomidae)

The vast majority of bats strongly depend on, but do not make, shelters or roosts. We investigated Lophostoma silvicolum, which roosts in active termite nests excavated by the bats themselves, to study the relationship between roost choice and mating systems. Due to the hardness of the termite nests, roost-making is probably costly in terms of time and energy for these bats. Video-observations and capture data showed that single males excavate nests. Only males in good physical condition attracted females to the resulting roosts. Almost all groups captured from excavated nests were single male-multifemale associations, suggesting a harem structure. Paternity assignments based on ten polymorphic microsatellites, revealed a high reproductive success of 46% by nest-holding males. We suggest that the mating system of L. silvicolum is based on a resource-defense polygyny. The temperatures in the excavated nests are warm and stable, and might provide a suitable shelter for reproductive females. Reproductive success achieved by harem males appears to justify the time and effort required to excavate the nests. Reproductive success may thus have selected on an external male phenotype, the excavated nests, and have contributed to the evolution of an otherwise rare behavior in bats.Communicated by G. Wilkinson     

Sex in the dark: determinants and consequences of mixed male mating tactics in<Emphasis Type="Italic"> Microcebus murinus</Emphasis>, a small solitary nocturnal primate

In mammals with solitary females, the potential for males to monopolize matings is relatively low, and scramble competition polygyny is presumed to be the predominant mating system. However, combinations of male traits and mating tactics within this type of polygyny have been described. The main aim of our study was to identify the relative importance of, and interactions among, potential determinants of contrasting male reproductive tactics, and to determine their consequences for male reproductive success in a small solitary nocturnal Malagasy primate, the gray mouse lemur (Microcebus murinus). We studied their mating behavior over three consecutive annual mating seasons. In addition, we determined the genetic relationships among more than 300 study animals to quantify the reproductive success of individual males. We found that, with a given relatively low overall monopolization potential, successful male mouse lemurs roamed extensively in search of mates, had superior finding ability and mated as early as possible. However, contest competition was important too, as temporary monopolization was also possible. Males exhibited different mating tactics, and heavier males had a higher reproductive success, although most litters had mixed paternities. Switching between tactics depended on short-term local variation in monopolization potential determined by a pronounced dynamic in fertilization probability, number of alternative mating opportunities, and the operational sex ratio. This study also revealed that the dynamics of these determinants, as well as the mutual interactions between them, necessitate a detailed knowledge of the mating behavior of a species to infer the impact of determinants of alternative mating tactics.Electronic Supplementary Material Supplementary material is available in the online version of this article at Communicated by S. AlbertsThis revised version was published online in August 2004 with corrections to Figure 2.     

Increased sperm numbers in the vas deferens of meadow voles, <Emphasis Type="Italic">Microtus pennsylvanicus,</Emphasis> in response to odors of conspecific males

Sperm competition occurs when the sperm of two or more males compete to fertilize the egg/s of a particular female. Males of some species respond to a high risk of sperm competition by increasing the number of sperm in their ejaculates. Males may accomplish such a response by increasing the intensity or duration of contraction of the cauda epididymidis and vas deferens. During emission (first phase of the ejaculatory process), the vas deferens receives sperm from the cauda epididymidis and propels the sperm to the urethra. In this paper, we tested the hypothesis that males exposed to a high risk of sperm competition mobilize larger numbers of sperm from the cauda epididymidis to the vas deferens before initiation of copulatory behavior. This accumulation of sperm in the vas deferens would result in a larger number of sperm in the ejaculate. To test this hypothesis, we exposed male meadow voles, Microtus pennsylvanicus, to either low or high risks of sperm competition using soiled bedding of conspecific individuals. At three different times after this exposure (15, 30, or 60 min), we removed both vasa deferentia and counted the sperm within them. We found a significant increase in sperm numbers in the vas deferens of males after 30 min of being exposed to a high risk of sperm competition. The lower sperm numbers after 15 and 60 min of exposure suggest that the observed response is relatively slow and that sperm mobilized to the vasa deferentia may return to the cauda epididymides if ejaculation does not occur some time after the observed response. Our results indicate that the physiological response that may result in high sperm numbers in the ejaculate in relation to high risk of sperm competition can occur before initiation of copulatory behavior.     

Sequential male mate choice in a fish,the Pacific blue-eye<Emphasis Type="Italic"> Pseudomugil signifer</Emphasis>

Mate choice is not just a female preoccupation. Under some circumstances, males may also be choosy. However, studies of male mate choice have generally been confined to situations where males can make direct comparisons between potential partners. In contrast, sequential male mate choice has largely been overlooked despite its biologically importance, especially if current investment in mate attraction diminishes a males future mating opportunities. Using the Pacific blue-eye fish Pseudomugil signifer, we show that males are capable of exercising sequential mate choice. When presented sequentially with large and small females, males spent more effort courting the former. However, males did not appear to modify the time spent courting a given female based on the size of the female encountered previously. We suggest that greater attention to the sequential choice problem in males may help illuminate similarities and differences between the sexes when it comes to mating decisions.Communicated by T. Czeschlik     

Divergence in female calling song discrimination between sympatric and allopatric populations of the southern wood cricket Gryllus fultoni (Orthoptera: Gryllidae)

Two species of closely related wood cricket, Gryllus fultoni (Orthoptera: Gryllidae) and Gryllus vernalis, occur together in some parts of the eastern United States and have a similar calling song structure, consisting of three-pulse chirps. A previous study revealed that chirp rate in G. fultoni was highest (greatest difference vis-à-vis chirp rate in G. vernalis) in sympatric populations, intermediate in near allopatric populations that were located close to the sympatric zone, and lowest in allopatric populations. A similar trend was observed in pulse rate, but the mean values of this trait showed much more convergence than chirp rate at the low end of the range of calling temperatures. In this study, we investigated the song discrimination of females from sympatric and allopatric populations of G. fultoni at about 23°C, which is near the middle of the normal range of calling temperatures. We used both single-stimulus and two-stimulus playback experiments to learn if geographical differences in song preferences paralleled those in calling songs. Stimuli presented were representative of calling songs in three classes of G. fultoni populations (sympatric, near allopatric, and far allopatric), a calling song of G. vernalis, and three calling songs with parameter values that were intermediate with respect to those of the songs of far allopatric G. fultoni and G. vernalis. In the single-stimulus playbacks, females of all G. fultoni populations responded poorly if at all to the heterospecific stimulus. Females of sympatric and near allopatric populations responded poorly to all intermediate stimuli, but females of far allopatric populations frequently responded to these sounds. In the two-stimulus playbacks, females of sympatric and near allopatric populations generally discriminated against intermediate and heterospecific stimuli. However, females of far allopatric populations often did not discriminate against intermediate stimuli, whose characteristics resembled the calling songs of G. vernalis. The divergent pattern of female phonotactic discrimination between sympatric and far allopatric populations was thus generally congruent with the pattern of divergence in chirp and pulse rates and would be expected to significantly reduce heterospecific mating in sympatry. These geographical patterns of female song discrimination and male calling songs conform to a commonly used definition of reproductive character displacement.     

Maintenance of variance in sperm transfer rates in a scorpionfly: food availability,genetic basis,and heritability

Variation in traits closely related to fitness is expected to be low. This is because these traits are under directional selection and the best genotype should prevail. However, there have been a number of studies demonstrating the existence of considerable variance in sexually selected traits, which is generally known as the lek paradox. Accordingly, earlier studies found substantial variation in sperm transfer rates in Panorpa vulgaris. Aiming at finding the mechanism that maintains this variation, we analyzed the condition dependence and the narrow sense heritability of sperm transfer rates. Food deprivation in the larval/adult phase caused a decrease in the males’ capability of saliva secretion resulting in shorter copulations and a reduced number of transferred sperm. There was a positive correlation between mean sperm transfer rates and mean body mass. Additionally, intermale variation in sperm transfer rates decreased with increasing food availability. Hence, we suggest that sperm transfer rates in P. vulgaris are influenced by adult feeding history. Heritability analyses of sperm transfer rates did not provide significant results, which is consistent with the general hypothesis that additive genetic variance in traits closely related to fitness is small. Since a trait’s potential to respond to selection is proportional to the amount of contained additive genetic variance, the ascertained small heritability provides a satisfying explanation for the maintenance of substantial variation in sperm transfer rates.     

The lemur syndrome unresolved: extreme male reproductive skew in sifakas (<Emphasis Type="Italic">Propithecus verreauxi</Emphasis>), a sexually monomorphic primate with female dominance

The primates of Madagascar (Lemuriformes) are unusual among mammals in that polygynous species lack sexual dimorphism, and females dominate males socially in most species. Moreover, lemur groups are relatively small and characterized by even adult sex ratios despite the fact that one male should be able to exclude other males from the group. One hypothesis to explain this combination of behavioral, morphological, and demographic traits (the “lemur syndrome”) postulates that male–male competition is relaxed and, hence, variance in male reproductive success is low. Reproductive skew theory provides a framework for testing this and several related predictions about lemur social evolution. Specifically, low reproductive skew is also predicted if dominant males or adult females make reproductive concessions to subordinates or if the latter group successfully pursues alternative reproductive tactics. However, suitable data on paternity, demography, and behavior for a conclusive test of these predictions have not been available in the past. In this paper, we show that male reproductive success in ten groups of Verreaux’s sifakas (Propithecus verreauxi) was extremely skewed in favor of the dominant male over 9 years. Our genetic analyses also revealed that more than a third of all groups are effectively harem groups because only one male was unrelated to the resident female(s). In groups with two or more non-natal males, the dominant sired 91% of 33 infants. Together, males pursuing one of several alternative reproductive tactics, such as roaming among several groups or immigrating peacefully, sired only 11% of infants. Thus, female sifakas do not control group composition by offering reproductive opportunities to subordinate males as staying incentives, intrasexual selection is not relaxed, and dominant males prevail in a tug-of-war over subordinate males. Because male reproductive skew in sifakas is even more pronounced than in harem-living anthropoids studied to date, intrasexual selection is clearly not relaxed, and the lemur syndrome is more puzzling than ever.     

Reproductive success of male bank voles (<Emphasis Type="Italic">Clethrionomys glareolus</Emphasis>): the effect of operational sex ratio and body size

The operational sex ratio (OSR) may influence the intensity of competition for mates and mate choice and is therefore thought to be a major factor predicting the intensity and direction of sexual selection. We studied the opportunity for sexual selection, i.e., the variance in male reproductive success and the direction and intensity of sexual selection on male body mass in bank vole (Clethrionomys glareolus) enclosure populations with experimentally manipulated sex ratios. The opportunity for sexual selection was high among male-biased OSRs and decreased towards female-biased OSRs. Paradoxically, selection for large male body mass was strongest in female-biased OSRs and also considerable at intermediate OSRs, whereas at male-biased OSRs, only a weak relationship between male size and reproductive success was found. Litters in male-biased OSRs were more likely to be sired by multiple males than litters in female-biased OSRs. Our results suggest that the intensity and direction of sexual selection in males differs among different OSRs. Although the direction of sexual selection on male body mass was opposite than predicted, large body mass can be favored by sexual selection. Naturally varying OSRs may therefore contribute to maintain variation in male sexually selected traits.