Costs of mating competition limit male lifetime breeding success in polygynous mammals

Although differences in breeding lifespan are an important source of variation in male fitness, the factors affecting the breeding tenure of males have seldom been explored. Here, we use cross-species comparisons to investigate the correlates of breeding lifespan in male mammals. Our results show that male breeding lifespan depends on the extent of polygyny, which reflects the relative intensity of competition for access to females. Males have relatively short breeding tenure in species where individuals have the potential to monopolize mating with multiple females, and longer ones where individuals defend one female at a time. Male breeding tenure is also shorter in species in which females breed frequently than in those where females breed less frequently, suggesting that the costs of guarding females may contribute to limiting tenure length. As a consequence of these relationships, estimates of skew in male breeding success within seasons overestimate skew calculated across the lifetime and, in several polygynous species, variance in lifetime breeding success is not substantially higher in males than in females.     

Male mating success, reproductive success and multiple paternity in a natural population of sand lizards: behavioural and molecular genetics data

Sand lizard Lacerta agilis females characteristically mate with several males which, in staged mating experiments, results in multiple paternity of the offspring. In order to investigate multiple paternity in a natural population and interpret male reproductive behaviours in terms of sired young, we sampled the blood of females, potential fathers and hatchlings, and determined paternity using multilocus DNA fingerprinting as well as the variation at a single locus detected by the probe (TC) _n . The paternity analyses were preceded by a laboratory experiment in which we established that the parental alleles identified by the single locus probe were inherited in a Mendelian way. Our molecular data demonstrated that 12 out of 13 males (92%) that sired offspring were correctly identified from the 56 sexually mature males in the population. Also smaller males were accepted as sexual partners by the females, but sired fewer young in competition with larger males and were less able to maintain prolonged post-copulatory mate guarding. This may result in that some sexually successful males are only observed inside a female's home range, but never in pair-association with the female.     

Relationship between female mating strategy, litter success and offspring dispersal

The relationship between mating systems and dispersal has generally been studied at the population and species levels. It has hardly ever been investigated at the individual level, by studying the variations of mating and dispersal strategies between individuals. We investigated this relationship in a natural population of the common lizard ( Lacerta vivipara ). Assuming that dispersal has a genetic basis, juvenile dispersal would be expected to be more family-dependent in monoandrous litters than in polyandrous litters. The opposite pattern was observed. Thus, maternal effects and/or litter effects play a greater role than genetic determinism in shaping the dispersal phenotype of juveniles. Moreover, the relationship between female mating strategy and offspring dispersal depended on litter success, in a way consistent with an influence of mother-offspring competition. Such a link between mating and dispersal strategies of individuals may have major repercussions for the way we consider the roles of these processes in population functioning.     

Male emergence timing and mating success in the funnel-web spider,Agelena limbata (Araneae: Agelenidae)

Field observations on the relationship between male mating success and emergence timing in the funnel-web spider,Agelena limbata, were conducted.Agelena limbata is an annual species and adult males appear slightly earlier than adult females in July. As males deposit a copulatory plug at the female epigynum after copulation, copulation with virgin females is important to males. The number of copulations in males with virgin females, which strongly correlates with the longevity of males and the number of females that males courted, did not correlate with the emergence timing of males. Early emerged males and females were significantly larger in size than later ones, but the correlation coefficient between the emerged date and the cephalothorax width was not strong. Males that emerged earlier did not have any advantage in copulating with larger and more fecund females. Furthermore, virgin females first copulated on average 7.9 days after their final molt and the mortality rate of adult males increased after the final molt. These factors may favor the smaller degree of protandry in male emergence timing inA. limbata.     

Male-male competition and mating success in the orb-web spider,Nephila clavata,with reference to temporal factors

Seasonal occurrence patterns of adults of both sexes, intensity of male-male interactions, and mating success in the spider,Nephila clavata, were examined in the field. Adult males began to attend female webs about 2 weeks before female maturation. Large adult males were abundant in the early breeding season, but small males increased later in the season. From the distribution of males among female webs and size relationship of males within a web, male-male interactions seemed to be more intense when most females were still subadult. This was verified by a field experiment in which males were artificially introduced to female webs that were attended by other males. It was found that the probability of introduced males remaining on subadult female webs was lower than that on adult webs. As mating occurred mostly in the period shortly after the female final molt and first male sperm precedence was known in all spiders reported so far, intense male-male competition on subadult female webs seemed to be reasonable. Male longevity had an important influence on the mating success of males with just-molted females. Mating success was also affected by the relative body size of males present in a given period. Since larger males occupied the position closest to females within a web and stayed there longer, relative body size appeared to influence mating success through male-male competition. Female body size at maturation declined with time; hence, males that attained sexual maturity earlier had the advantage of mating with larger and more fecund females. Therefore, early maturation as well as larger size seem to be two important trairs influencing the reproductive success of males.     

Influences of mating groups on the reproductive success of the Southern Sichuan Red Panda (Ailurus fulgens styani)

The reproduction of female red pandas under three different husbandry conditions (monogamy, polygamy, and polyandry) was studied at the Chengdu Research Base for Giant Panda Breeding, and Chengdu Zoological Park, China. We monitored the fecal steroid profiles of seven females by radioimmunoassay in order to understand how the different mating groupings affect the animals' reproductive success. Of the seven females studied, all gave birth except the one that was kept in the polyandrous group. Although fecal estradiol metabolites exhibited several peaks during estrus, only one coincided with mating behavior. Fecal progesterone metabolites did not display a sustained rise in the absence of mating behavior, even though estradiol displayed a peak of secretion. This suggests that the red panda may be an induced ovulator. During gestation, fecal progesterone metabolites were maintained at a comparatively high level, and were much higher than those of nonpregnant females. The female in the polyandrous group showed an abnormal estradiol metabolite profile, with a level that was four to five times higher than those of the females in the polygynous groupings. It was observed that this female always escaped and hid in the trees to avoid courtships with males, and did not give birth. This phenomenon suggests that polyandrous groupings may be unsuitable for successful reproduction in captivity. Zoo Biol 24:169–176, 2005. © 2005 Wiley‐Liss, Inc.     

High levels of multiple paternity in a spermcast mating freshwater mussel

Multiple paternity is an important characteristic of the genetic mating system and common across a wide range of taxa. Multiple paternity can increase within‐population genotypic diversity, allowing selection to act on a wider spectre of genotypes, and potentially increasing effective population size. While the genetic mating system has been studied in many species with active mating behavior, little is known about multiple paternity in sessile species releasing gametes into the water. In freshwater mussels, males release sperm into the water, while eggs are retained and fertilized inside the female (spermcast mating). Mature parasitic glochidia are released into the water and attach to the gills of fish where they are encapsulated until settling in the bottom substrate. We used 15 microsatellite markers to detect multiple paternity in a wild population of the freshwater pearl mussel (Margaritifera margaritifera). We found multiple paternity in all clutches for which more than two offspring were genotyped, and numbers of sires were extremely high. Thirty‐two sires had contributed to the largest clutch (43 offspring sampled). This study provides the first evidence of multiple paternity in the freshwater pearl mussel, a species that has experienced dramatic declines across Europe. Previous studies on other species of freshwater mussels have detected much lower numbers of sires. Multiple paternity in freshwater pearl mussels may be central for maintaining genetic variability in small and fragmented populations and for their potential to recover after habitat restoration and may also be important in the evolutionary arms race with their fish host with a much shorter generation time.     

Multiple mating and its effect on the reproductive success of female Epiphyas postvittana (Lepidoptera: Tortricidae)

Abstract.

• 1 Multiple mating and its effect on reproductive performance of female Epiphyas postvittana (Walker) moths were studied under controlled conditions.
• 2 The age at which the moths mated for the first time ranged from the first to the tenth day after emergence, but 71% of first matings were during the first 3 days.
• 3 The majority (63%) of females had one or two spermatophores in the bursa copulatrix. Some (24%) were found with three to five spermatophores, whereas no successful mating occurred among 13% of individuals. The number of matings was partly dependent on the number of mates available to the female. Between the range of sex ratios of one male to one female and four males to one female maximal mating success occurred at the ratio of three males to one female.
• 4 Virgin females were capable of egg-laying, but mating stimulated and accelerated oviposition. Mated individuals laid twice as many eggs as unmated ones.
• 5 The level of copulatory activity did not influence the longevity of females irrespective of the number of males available to them.
• 6 Sex ratios with greater than one male to a female improved the reproductive success by marginally increasing fecundity and fertility.
• 7 It is concluded that multiple mating would enhance population growth, and is of particular benefit to populations with a preponderance of females, as is known to occur naturally in this species.

     

Effects of fine‐scale genetic structure on male mating success in gynodioecious Beta vulgaris ssp. maritima

Plant mating systems are known to influence population genetic structure because pollen and seed dispersal are often spatially restricted. However, the reciprocal outcomes of population structure on the dynamics of polymorphic mating systems have received little attention. In gynodioecious sea beet (Beta vulgaris ssp. maritima), three sexual types co‐occur: females carrying a cytoplasmic male sterility (CMS) gene, hermaphrodites carrying a non‐CMS cytoplasm and restored hermaphrodites that carry CMS genes and nuclear restorer alleles. This study investigated the effects of fine‐scale genetic structure on male reproductive success of the two hermaphroditic forms. Our study population was strongly structured and characterized by contrasting local sex‐ratios. Pollen flow was constrained over short distances and depended on local plant density. Interestingly, restored hermaphrodites sired significantly more seedlings than non‐CMS hermaphrodites, despite the previous observation that the former produce pollen of lower quality than the latter. This result was explained by the higher frequency of females in the local vicinity of restored (CMS) hermaphrodites as compared to non‐CMS hermaphrodites. Population structure thus strongly influences individual fitness and may locally counteract the expected effects of selection, suggesting that understanding fine scale population processes is central to predicting the evolution of gender polymorphism in angiosperms.     

Breeding success of male brook trout (Salvelinus fontinalis) in the wild

Competition for females generally results in some males adopting alternative reproductive tactics to acquire matings. For fish, the ecological and evolutionary consequences of these tactics are not well understood because of an inability to link directly the interactions of individuals on the breeding grounds with genetic data. This study combines behavioural observations with genetic estimates of male reproductive success within an intensively studied wild population of lacustrine brook trout (Salvelinus fontinalis). Male brook trout exhibit a conditional reproductive strategy with small males adopting a peripheral position to that of larger dominant males in their proximity to spawning females. Parentage analysis of eggs collected from wild redds confirmed the reproductive success of individual males. Males relegated to peripheral positions during spawning participated frequently in spawning events, but in most cases the first male to spawn was the sole contributor, and no more than two males contributed successfully to a single brood. While behavioural observations of salmonines suggests that reproduction is partitioned among males in a manner dependent upon body size and proximity to spawning females, the genetic evidence from this study suggests a more limited distribution of reproductive success in the field. The genetic contributions of male brook trout are highly skewed towards larger males for this population. A review of the salmonine literature suggests little difference in individual reproductive success for males exhibiting size-related tactics within a conditional mating strategy vs. precocial maturation. Collectively, these genetic studies provide new insights on the evolution of alternative life histories among salmonines.     

A field observation on the influence of aggressive behaviour on mating success in the European grayling

The biggest male grayling present on a spawning area was strongly territorial and developed more aggressive behaviours than smaller males. However, its spawning frequency was similar to that of Smaller males.     

Impact of male mating history on the postmating resumption of sexual receptivity and lifetime reproductive success in Choristoneura rosaceana females

Abstract.  The first objective of the present study is to test the hypothesis that the decrease in the number of eupyrene spermatozoa in the spermatheca is directly associated with the resumption of sexual receptivity in female moths, an aspect that has not been examined in previous studies. The obliquebanded leafroller, Choristoneura rosaceana , is used and females mated with previously mated males have a shorter refractory period than those mated with virgins. This difference is associated with a faster rate of movement of sperm from the spermatheca. Overall, the length of the female refractory period coincides with the mean time required for the number of eupyrene sperm in the spermatheca to drop to approximately 3000, regardless of male mating history. Although such a decline in sperm numbers may be a factor responsible for the resumption of sexual receptivity, this is clearly not the only one because more than 40% of females remate even though sperm numbers in the spermatheca are well above this threshold. Virgin males do not vary the mass or the content of their ejaculate as a function of the female's reproductive status and this may increase the risk of sperm competition if the female is previously mated. The second objective of this study is to examine the effect of previous male mating history on female reproductive potential. Females mated with previously mated males have a significantly lower fecundity than those mated with virgin males. However, in all treatments, remating increases both female longevity and lifetime fecundity. There is also a significant effect of female mass on the length of the refractory period and on lifetime fecundity, with large females resuming sexual receptivity sooner and laying more eggs than small ones, regardless of male mating history.     

Reproductive success and effective population size in woodrats (Neotoma macrotis)

Discrepancies between the census size and the genetically effective size of populations (N(e)) can be caused by a number of behavioural and demographic factors operating within populations. Specifically, strong skew in male reproductive success, as would be expected in a polygynous mating system, could cause a substantial decrease in N(e) relative to census size. Because the mating system of Neotoma macrotis had previously been described as one nearing harem polygyny, I examined the distribution of reproductive success and genetic variation within a population of this species. Combining genetic data and three years of field observations, I show that variance in reproductive success does not deviate from poisson expectations within either sex and variance in success is similar between the sexes. Furthermore, both males and females had multiple partners across litters in addition to some evidence of multiple paternity within litters. Despite a lack of strong skew in reproductive success, an estimate of N(e) based on a number of demographic parameters suggests that the ratio of N(e)/N in this population is 0.48. Although the ratio of N(e)/N suggests that the population is experiencing higher rates of genetic drift than would be expected based on census size alone, the population maintains high levels of genetic diversity. Estimates of neighbourhood size and patterns of recruitment to the study site suggest that immigration plays an important role in this population and may contribute to the maintenance of high levels of genetic diversity.     

The contribution of multiple mating and spermatophore consumption to the lifetime reproductive success of female field crickets (Gryllus bimaculatus)

ABSTRACT.

• 1 The adaptive significance of multiple mating by female Gryllus bimaculatus (De Geer) was investigated.
• 2 Multiple mating prevented the depletion of sperm stores and, therefore, maintained high hatching success. This may not, however, explain the high frequency of remating in this species.
• 3 Male-derived egg stimulants known to be passed with sperm at mating increased the number of eggs produced only when females mated throughout their lifespans.
• 4 Spermatophore consumption appeared to provide nutrients which, while they did not increase the quantity of eggs, increased egg quality as indicated by weight. Females who consumed spermatophores had a greater hatching success.
• 5 While females may derive non-genetic benefits from mating, these are apparently long-term benefits; females must mate throughout their lives in order to accrue them.
• 6 Since the benefits of mating may not be derived from individual males, the spermatophores and their contents in this species are best considered as mating effort.

     

Patterns of male reproductive success in a highly promiscuous whale species: the endangered North Atlantic right whale

Parentage analyses of baleen whales are rare, and although mating systems have been hypothesized for some species, little data on realized male reproductive success are available and the patterns of male reproductive success have remained elusive for most species. Here we combine over 20 years of photo-identification data with high-resolution genetic data for the majority of individual North Atlantic right whales to assess paternity in this endangered species. There was significant skew in male reproductive success compared to what would be expected if mating was random (P < 0.001). The difference was due to an excess of males assigned zero paternities, a deficiency of males assigned one paternity, and an excess of males assigned as fathers for multiple calves. The variance in male reproductive success was high relative to other aquatically mating marine mammals, but was low relative to mammals where the mating system is based on resource- and/or mate-defence polygyny. These results are consistent with previous data suggesting that the right whale mating system represents one of the most intense examples of sperm competition in mammals, but that sperm competition on its own does not allow for the same degree of polygyny as systems where males can control access to resources and/or mates. The age distribution of assigned fathers was significantly biased towards older males (P < 0.05), with males not obtaining their first paternity until approximately 15 years of age, which is almost twice the average age of first fertilization in females (8 years), suggesting that mate competition is preventing younger males from reproducing. The uneven distribution of paternities results in a lower effective population size in this species that already has one of the lowest reported levels of genetic diversity, which may further inhibit reproductive success through mate incompatibility of genetically similar individuals.     

Mating system and reproductive success in eastern Pacific harbour seals

Harbour seals sometimes breed along inland travel corridors where females become clustered in space and time and males establish underwater acoustic display territories similar to terrestrial arenas known as resource-based leks. Under these conditions, we predicted that higher levels of polygyny would be observed than has been previously reported for this species mating in open coast environments without travel corridors. Reproductive success (RS) of 70 males was measured using 20 microsatellite DNA loci and likelihood-based paternity analysis of 136 offspring collected over 3 years. Most males were assigned either zero or one paternity with 80% confidence. The greatest number of pups assigned to one male in a season was two. Variance in RS was higher for males than females (which are biologically limited to one offspring per year) indicating low to mild polygyny. In addition, distributions of relatedness values among pups within year classes did not differ significantly from a simulated distribution with R = 0, indicating that half-siblings were uncommon. Overall, polygyny levels were low relative to terrestrial pinniped mating systems and similar to observations from a harbour seal population along an open coast. Due to large confidence intervals associated with our results, we cannot rule out the hypothesis that a travel corridor might increase the degree of polygyny skew relative to that observed in open coast environments. Habitat appeared to influence male strategies as the most successful males in open coast environments patrolled offshore, while the most successful male in this study defended a territory along the travel corridor.     

Effect of mating frequency and brood cell infestation rate on the reproductive success of the honeybee parasite Varroa jacobsoni

Abstract.

• 1 The reproductve biology of Varroa jacobsoni, whose females infest honeybee brood, was studied in natural and transparent artificial brood cells. These investigations were made under the headings of maturation behaviour and fertilization, and the influence of infestation rate of brood cells on the number of mated females produced per infesting Varroa.
• 2 Mating of Varroa daughters, observed in the transparent brood cells with time-lapse video, occurs just after ecdysis and as soon as they arrive on the faecal accumulation prepared by the mother. Such females are remated for as long as no other freshly moulted daughter arrives on the faecal accumulation.
• 3 The number of spermatozoa stocked in the spermatheca increases with remating, a strong indication for sperm mixing in this species when brood cells contain more than one Varroa foundress.
• 4 The number of daughters per infesting mother decreases at higher rates of infestation per cell, but the proportion of such daughters with a mate rises sharply due to the higher probability of finding a male within multi-infested cells. The number of mated daughters per mother is maximal in cells with two foundress Varroa females.
• 5 The frequency distributions of infesting mites in drone cells are aggregated, and approximate to negative binomial distributions.
• 6 We postulate from the above that the observed non-random infestation by Varroa in drone brood augments the mite's mean reproductive success through the production of a higher number of mated daughters than the corresponding Poisson distributions would.