Conflict over multiple-partner mating between males and females of the polygynandrous common lizards

The optimal number of mate partners for females rarely coincides with that for males, leading to a potential sexual conflict over multiple-partner mating. This suggests that the population sex ratio may affect multiple-partner mating and thus multiple paternity. We investigate the relationship between multiple paternity and the population sex ratio in the polygynandrous common lizard (Lacerta vivipara). In six populations the adult sex ratio was biased toward males, and in another six populations the adult sex ratio was biased toward females, the latter corresponding to the average adult sex ratio encountered in natural populations. In males the frequency and the degree of polygyny were lower in male-biased populations, as expected if competition among males determines polygyny. In females the frequency of polyandry was not different between treatments, and polyandrous females produced larger clutches, suggesting that polyandry might be adaptive. However, in male-biased populations females suffered from reduced reproductive success compared to female-biased populations, and the number of mate partners increased with female body size in polyandrous females. Polyandrous females of male-biased populations showed disproportionately more mating scars, indicating that polyandrous females of male-biased populations had more interactions with males and suggesting that the degree of multiple paternity is controlled by male sexual harassment. Our results thus imply that polyandry may be hierarchically controlled, with females controlling when to mate with multiple partners and male sexual harassment being a proximate determinant of the degree of multiple paternity. The results are also consistent with a sexual conflict in which male behaviors are harmful to females.     

The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus)

Sexual selection is an important force driving the evolution of morphological and genetic traits. To determine the importance of male-male, postcopulatory sexual selection in natural populations of house mice, we estimated the frequency of multiple paternity, defined as the frequency with which a pregnant female carried a litter fertilized by more than one male. By genotyping eight microsatellite markers from 1095 mice, we found evidence of multiple paternity from 33 of 143. Evidence for multiple paternity was especially strong for 29 of these litters. Multiple paternity was significantly more common in higher-density vs. lower-density populations. Any estimate of multiple paternity will be an underestimate of the frequency of multiple mating, defined as the frequency with which a female mates with more than a single male during a single oestrus cycle. We used computer simulations to estimate the frequency of multiple mating, incorporating observed reductions in heterozygosity and levels of allele sharing among mother and father. These simulations indicated that multiple mating is common, occurring in at least 20% of all oestrus cycles. The exact estimate depends on the competitive skew among males, a parameter for which we currently have no data from natural populations. This study suggests that sperm competition is an important aspect of postcopulatory sexual selection in house mice.     

Operational sex ratio, sexual conflict and the intensity of sexual selection

Modern sexual selection theory indicates that reproductive costs rather than the operational sex ratio predict the intensity of sexual selection. We investigated sexual selection in the polygynandrous common lizard Lacerta vivipara . This species shows male aggression, causing high mating costs for females when adult sex ratios (ASR) are male-biased. We manipulated ASR in 12 experimental populations and quantified the intensity of sexual selection based on the relationship between reproductive success and body size. In sharp contrast to classical sexual selection theory predictions, positive directional sexual selection on male size was stronger and positive directional selection on female size weaker in female-biased populations than in male-biased populations. Thus, consistent with modern theory, directional sexual selection on male size was weaker in populations with higher female mating costs. This suggests that the costs of breeding, but not the operational sex ratio, correctly predicted the strength of sexual selection.     

Experimental evolution reveals trade-offs between mating and immunity

Immune system maintenance and upregulation is costly. Sexual selection intensity, which increases male investment into reproductive traits, is expected to create trade-offs with immune function. We assayed phenoloxidase (PO) and lytic activity of individuals from populations of the Indian meal moth, Plodia interpunctella, which had been evolving under different intensities of sexual selection. We found significant divergence among populations, with males from female-biased populations having lower PO activity than males from balanced sex ratio or male-biased populations. There was no divergence in anti-bacterial lytic activity. Our data suggest that it is the increased male mating demands in female-biased populations that trades-off against immunity, and not the increased investment in sperm transfer per mating that characterizes male-biased populations.     

Constrained sex allocation in a parasitoid due to variation in male quality

The theory of constrained sex allocation posits that when a fraction of females in a haplodiploid population go unmated and thus produce only male offspring, mated females will evolve to lay a female-biased sex ratio. I examined evidence for constrained sex ratio evolution in the parasitic hymenopteran Uscana semifumipennis. Mated females in the laboratory produced more female-biased sex ratios than the sex ratio of adults hatching from field-collected eggs, consistent with constrained sex allocation theory. However, the male with whom a female mated affected her offspring sex ratio, even when sperm was successfully transferred, suggesting that constrained sex ratios can occur even in populations where all females succeed in mating. A positive relationship between sex ratio and fecundity indicates that females may become sperm-limited. Variation among males occurred even at low fecundity, however, suggesting that other factors may also be involved. Further, a quantitative genetic experiment found significant additive genetic variance in the population for the sex ratio of offspring produced by females. This has only rarely been demonstrated in a natural population of parasitoids, but is a necessary condition for sex ratio evolution. Finally, matings with larger males produced more female-biased offspring sex-ratios, suggesting positive selection on male size. Because the great majority of parasitic hymenoptera are monandrous, the finding of natural variation among males in their capacity to fertilize offspring, even after mating successfully, suggests that females may often be constrained in the sex allocation by inadequate number or quality of sperm transferred.     

Male mating behaviour and sperm production characteristics under varying sperm competition risk in guppies

Since natural populations of guppies, Poecilia reticulata, often differ from one another in social structure, the intensity of sperm competition is likely to vary between localities. Guppies are promiscuous, with female choice for colourful males playing a central role in the mating system. In addition, male guppies use forced copulations to circumvent female choice. Both methods of copulation are used interchangeably by individual males, but the degree to which either is used may depend on the social environment into which males are born. Here we show that male mating behaviour varies according to the rearing sex ratio: when reared in male-biased groups, males performed more forced copulations and fewer courtship displays but showed the opposite pattern of behaviour when reared in female-biased groups. Our prediction, based on sperm competition theory, that stripped sperm number would reflect social structure was not supported by our results. Instead, the overall level of sexual activity (gonopodial thrusts+sigmoid displays) was a better predictor of sperm number in the different groups of males. Rearing density, where sex ratio was controlled, did not significantly affect male mating behaviour or sperm traits. Males reared under the different sex ratios continued to show their characteristic behaviour patterns when placed in equal sex ratio tanks. We conclude, therefore, that males adopt mating strategies to suit their social environment, and that these strategies remain fixed, for short periods at least, if population structure changes. Copyright 1999 The Association for the Study of Animal Behaviour.     

Sex allocation predicts mating rate in a simultaneous hermaphrodite

Sexual selection theory for separate-sexed animals predicts that the sexes differ in the benefit they can obtain from multiple mating. Conventional sex roles assume that the relationship between the number of mates and the fitness of an individual is steeper in males compared with females. Under these conditions, males are expected to be more eager to mate, whereas females are expected to be choosier. Here we hypothesize that the sex allocation, i.e. the reproductive investment devoted to the male versus female function, can be an important predictor of the mating strategy in simultaneous hermaphrodites. We argue that within-species variation in sex allocation can cause differences in the proportional fitness gain derived through each sex function. Individuals should therefore adjust their mating strategy in a way that is more beneficial to the sex function that is relatively more pronounced. To test this, we experimentally manipulated the sex allocation in a simultaneously hermaphroditic flatworm and investigated whether this affects the mating behaviour. The results demonstrate that individuals with a more male-biased sex allocation (i.e. relatively large testes and small ovaries) are more eager to mate compared with individuals with a more female-biased sex allocation (i.e. relatively small testes and large ovaries). We argue that this pattern is comparable to conventional gender roles in separate-sexed organisms.     

Genetic monogamy despite social promiscuity in the pot-bellied seahorse (Hippocampus abdominalis)

Sexual selection theory predicts a positive correlation between relative parental investment and mate choice. In syngnathid fishes (seahorses and pipefish), males brood offspring in specialized brooding structures. While female-female mating competition has been demonstrated in some pipefishes, all seahorses (genus Hippocampus) studied to date have been found to have conventional sex roles with greater male-male competition for access to mates despite possessing the most complex brood structures in the family. Although multiple mating is common in pipefish, seahorses are again exceptional, exhibiting strict genetic monogamy. Both demographic and behavioural explanations have been offered to explain the lack of multiple mating in seahorse species, but these hypotheses have not yet been explicitly addressed. We investigated mating systems and brood parentage of the pot-bellied seahorse, Hippocampus abdominalis, a temperate-water species that is socially promiscuous with conventional sex roles in laboratory populations. We observed promiscuous courtship behaviour and sex-role reversal in high density, female-biased field populations of H. abdominalis. We hypothesize that sex roles are plastic in H. abdominalis, depending on local population density and sex ratio. Despite promiscuous courtship behaviour, all assayed male seahorses were genetically monogamous in both laboratory and wild populations. Physiological limitations associated with embryo incubation may explain the absence of multiple mating in seahorses and may have played an important role in the development of the unique reproductive behaviour typical in these species.     

WHY DO SOME SOCIAL INSECT QUEENS MATE WITH SEVERAL MALES? TESTING THE SEX‐RATIO MANIPULATION HYPOTHESIS IN LASIUS NIGER

Although multiple mating most likely increases mortality risk for social insect queens and lowers the kin benefits for nonreproductive workers, a significant proportion of hymenopteran queens mate with several males. It has been suggested that queens may mate multiply as a means to manipulate sex ratios to their advantage. Multiple paternity reduces the extreme relatedness value of females for workers, selecting for workers to invest more in males. In populations with female-biased sex ratios, queens heading such male-producing colonies would achieve a higher fitness. We tested this hypothesis in a Swiss and a Swedish population of the ant Lasius niger. There was substantial and consistent variation in queen mating frequency and colony sex allocation within and among populations, but no evidence that workers regulated sex allocation in response to queen mating frequency; the investment in females did not differ among paternity classes. Moreover, population-mean sex ratios were consistently less female biased than expected under worker control and were close to the queen optimum. Queens therefore had no incentive to manipulate sex ratios because their fitness did not depend on the sex ratio of their colony. Thus, we found no evidence that the sex-ratio manipulation theory can explain the evolution and maintenance of multiple mating in L. niger.     

Variation in adult sex ratio alters the association between courtship, mating frequency and paternity in the lek-forming fruitfly Ceratitis capitata

The intensity with which males deliver courtship and the frequency with which they mate are key components of male reproductive success. However, we expect the strength of the relationship between these traits and a male's overall paternity to be strongly context dependent, for example to be altered significantly by the extent of post-mating competition. We tested this prediction in a lekking insect, Ceratitis capitata (medfly). We examined the effect of manipulating the sex ratio from male- to female-biased (high and low male competition, respectively) on courtship behaviour, mating frequency and paternity of focal males. Under high male competition, focal males delivered significantly more courtship but gained lower paternity than under lower competition. Paternity was positively associated with mating frequency and small residual testes size. However, the association between mating frequency and paternity was significantly stronger under low competition. We conclude that manipulation of sex ratio significantly altered the predictors of mating success and paternity. The relationship between pre- and post-mating success is therefore plastic and alters according to the prevailing level of competition. The results highlight the importance of post-copulatory processes in lekking species and illuminate selection pressures placed on insects such as medflies that are mass reared for pest control.     

Queen mating and paternity variation in the ant Lasius niger

We have electrophoretically analysed the variation in queen mating and worker paternity across and within seven populations of the ant Lasius niger in northwestern Europe. Populations were panmictic and not genetically differentiated ( F _ST = 0.003 ± 0.004; range c. 1000 km). Queens ( n = 535) were shown to mostly mate with a single male, but double mating occurred in all populations and triple mating was found in one case (the total number of worker offspring analysed for paternity was 4825). The genetically effective queen mating frequency was 1.16 on average across populations (range 1.04–1.42). Double sampling of six out of the seven populations showed that most of the variation in queen mating occurred among populations and not within populations among years. Also, paternity skew in colonies with double-mated queens was relatively constant per site but varied across populations. Paternity skew was high in populations with low frequencies of double queen-mating, low in populations with intermediate frequencies of double queen mating and ambiguous in a single population where more than half of the queens mated multiply. Double-mated queens were only collected halfway through a nuptial flight, suggesting that double mating is time consuming and that the mating swarm sex ratio may affect the likelihood of multiple mating towards the end of a flight. No difference in fresh weight between single- and double-mated queens from the same population was found.     

Female American mink, Mustela vison, mate multiply in a free-choice environment

Like most solitary carnivores, the home ranges of male American mink overlap with those of several females, but each female typically shares its range with only a single male. Nevertheless, female mink produce multiply sired litters. Unusually among mammals, the physiological characteristics of female American mink make them highly suited to multiple paternity, suggesting that polyandry in the species may result from female behaviour rather than from coercion by males. In a free-choice experiment on captive-bred animals, all female mink mated multiply, with seven of the eight mating with all three available partners. Since females sometimes resisted copulations, multiple mating in this species may result from their behaviour rather than male coercion. Females visited males nonrandomly, but visiting patterns did not predict mating patterns, suggesting disparate social and mating preferences. There was no evidence for precopulatory female choice, since the allocation of copulations among available males did not deviate significantly from the expected distribution. Females mated multiply only around the predicted times of ovulation, contrary to the expectation that they should be more selective at times of peak fertility. Larger males copulated for longer in total: copulation duration is probably under male control, suggesting that larger males could influence mating duration, perhaps increasing their share of paternity by greater sperm transfer. Our observations suggest that in wild populations, mating patterns could be influenced by female preference for multiple partners.     

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

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

Paternity success and the direction of sexual selection in a field population of a semelparous marsupial,Antechinus agilis

Antechinus agilis is a small sexually size dimorphic marsupial with a brief annual mating period of 2-3 weeks. All males die after this period, and females give birth to up to 10 young. Mating is thought to be promiscuous, however, there is no field data to confirm this. Using microsatellites, we investigated paternity patterns over two seasons in a wild population. Male weight was significantly positively related to the number of females fertilized and with the number of offspring sired, in both years. Furthermore, selection gradients indicated selection for larger males. Both results suggest that size dimorphism in A. agilis can be explained by sexual selection for larger males. The proportion of offspring sired within litters, did not relate to male size. Therefore, larger males are more successful through higher mating access, not through their sperm outcompeting that of smaller males. As expected from their known ranging behaviour, the number of offspring within litters left unassigned to a father did not depend on the grid location of the mother. Female size did not differ between successful reproducing and unsuccessful females. However, females that weaned offspring had larger heads than females that did not wean offspring. Males did not 'prefer' mating with larger females, nor did assortative mating occur. From our results, the mating system of A. agilis is clearly promiscuous. Selection for larger males occurred in both years, even though in one year the operational sex ratio was highly female biased, suggesting that the potential reproductive rate is a better predictor of the direction of sexual selection in A. agilis.     

Sexual size dimorphism and sexual selection in primates

1. In most animals, females are larger than males. Paradoxically, sexual size dimorphism is biased towards males in most mammalian species. An accepted explanation is that sexual dimorphism in mammals evolved by intramale sexual selection. I tested this hypothesis in primates, by relating sexual size dimorphism to seven proxies of sexual selection intensity: operational sex ratio, mating system, intermale competition, group sex ratio, group size, maximum mating percentage (percentage of observed copulations involving the most successful male), and total paternity (a genetic estimate of the percentage of young sired by the most successful male).
2. I fitted phylogenetic generalised least squares models using sexual size dimorphism as the dependent variable and each of the seven measures of intensity of sexual selection as independent variables. I conducted this comparative analysis with data from 50 extant species of primates, including Homo sapiens, Pan troglodytes, and Gorilla spp.
3. Sexual dimorphism was positively related to the four measures of female monopolisation (operational sex ratio, mating system, intermale competition, and group sex ratio) and in some cases to group size, but was not associated with maximum mating percentage or total paternity. Additional regression analyses indicated that maximum mating percentage and total paternity were negatively associated with group size.
4. These results are predicted by reproductive skew theory: in large groups, males can lose control of the sexual behaviour of the other members of the group or can concede reproductive opportunities to others. The results are also consistent with the evolution of sexual size dimorphism before polygyny, due to the effects of natural, rather than sexual, selection. In birds, the study of molecular paternity showed that variance in male reproductive success is much higher than expected by behaviour. In mammals, recent studies have begun to show the opposite trend, i.e. that intensity of sexual selection is lower than expected by polygyny.
5. Results of this comparative analysis of sexual size dimorphism and sexual selection intensity in primates suggest that the use of intramale sexual selection theory to explain the evolution of polygyny and sexual dimorphism in mammals should be reviewed, and that natural selection should be considered alongside sexual selection as an evolutionary driver of sexual size dimorphism and polygyny in mammals.

     

HOW WELL DO MATING FREQUENCY AND DURATION PREDICT PATERNITY SUCCESS IN THE POLYGYNANDROUS WATER STRIDER AQUARIUS REMIGIS?

Abstract.— The relationship between mating success and paternity success is a key component of sexual selection but has seldom been estimated for species in which both sexes mate with many partners (polygynandry). We used a modification of Parker's sterile male technique to measure this relationship for the water strider Aquarius remigis in 47 laboratory populations simulating natural conditions of polygynandry. We also tested the hypothesis that prolonged copulation, a characteristic of this species, enhances paternity success. Mating behavior and paternity success were assayed for four days while males and females freely interacted. Paternity success was also assayed for an additional 7 days when females were isolated from males. Mating success significantly predicted paternity success and accounted for ≤ 36% of the variance. Copulation duration was negatively related to both mating success and paternity success and did not explain any of the residual variance in paternity success. Thus, we found no evidence that prolonged copulation functions as a paternity assurance strategy in this species. Comparisons of sterile and fertile males suggested that paternity success is directly influenced by the quantity of sperm transferred. Our results support previous studies that have used mating success to estimate sexual selection, but also highlight the potential importance of sperm competition and other postinsemination processes.     

Further Mathematical Modelling of Mating Sex Ratios & Male Strategies with Special Relevance to Human Life History

Influential models of male reproductive strategies have often ignored the importance of mate guarding, focusing instead on trade-offs between fitness gained through care for dependants in a pair bond versus fitness from continued competition for additional mates. Here we follow suggestions that mate guarding is a distinct alternative strategy that plays a crucial role, with special relevance to the evolution of our own lineage. Human pair bonding may have evolved in concert with the evolution of our grandmothering life history, which entails a shift to male-biased sex ratios in the fertile ages. As that sex ratio becomes more male biased, payoffs for mate-guarding increase due to partner scarcity. We present an ordinary differential equation model of mutually exclusive strategies (dependant care, multiple mating, and mate guarding), calculate steady-state frequencies and perform bifurcation analysis on parameters of care and guarding efficiency. Mate guarding triumphs over alternate strategies when populations are male biased, and guarding is fully efficient. When guarding does not ensure complete certainty of paternity, and multiple maters are able to gain some paternity from guarders, multiple mating can coexist with guarding. At female-biased sex ratios, multiple mating takes over, unless the benefit of care to the number of surviving offspring produced by the mates of carers is large.     

Love the one you're with: proximity determines paternity success in the barnacle Tetraclita rubescens

A species' mating system sets limits on the strength of sexual selection. Sexual selection is widespread in dioecious species, but is less well documented in hermaphrodites, and may be less important. We used four highly polymorphic microsatellite markers to assign paternity to broods of the hermaphroditic eastern Pacific volcano barnacle Tetraclita rubescens. These data were used to describe the species' mating system and to examine factors affecting male reproductive success. Tetraclita can sire broods over distances of 11.2 cm, but proximity to the sperm recipient had a highly significant effect on the probability of siring success. There was no effect of body size or the mass of male reproductive tissues on siring success. Broods showed relatively low frequencies of multiple paternity; even at high densities, 75% of broods had only one father. High frequencies of single‐paternity broods imply either that this species does not compete via sperm displacement, or that sperm displacement is extremely effective, potentially explaining the lack of a positive relationship between male investment and paternity. In addition, there was low variance in siring success among individuals, suggesting a lack of strong sexual selection on male traits. Low variance among sires and the strong effect of proximity are probably driven by the unusual biology of a sessile copulating species.     

Density-related changes in sexual selection in red deer.

In sexually dimorphic mammals, high population density is commonly associated with increased mortality of males relative to females and with female-biased adult sex ratios. This paper investigates the consequences of these changes on the distribution of male breeding success, the intensity of competition for females and the opportunity for sexual selection. After the red deer (Cervus elaphus L.) population of the North Block of Rum (Inner Hebrides) was released from culling, female numbers rose and male numbers declined, leading to an adult sex ratio of around one male to two females. This change was the result of increased mortality of males relative to females during the first two years of life; of increased emigration rates by young males; and of reduced immigration by males from outside the study area. The increasing bias in the adult sex ratio affected the timing of breeding as well as the distribution of mating success in males. As the adult sex ratio became increasingly biased towards females, the degree of skew in mating success (calculated across all harem-holders) increased, but mature males defended harems for shorter periods and a higher proportion of males held harems. In addition, a higher proportion of calves were fathered by immigrant males and the proportion fathered by males born in the study area declined. These results support the contention that, where high population density is associated with a female-biased adult sex ratio, competition for mates is likely to decline.