Multiple mating and facultative polygyny in the Panamanian leafcutter ant Acromyrmex echinatior

Queen mating frequency of the facultatively polygynous ant Acromyrmex echinatior was investigated by analysing genetic variation at an (AG)_n repeat microsatellite locus in workers and sexuals of 20 colonies from a single Panamanian population. Thirteen colonies were found to be monogynous, 5 colonies contained multiple queens, whereas the queen number of 2 colonies remained unresolved. Microsatellite genotypes indicated that 12 out of 13 queens were inseminated by multiple males (polyandry). The mean queen mating frequency was 2.53 and the mean genetically effective paternity frequency was 2.23. These values range among the highest found in ants, and the results are in keeping with the high mating frequencies reported for other species of leafcutter ants. Consistent skew in the proportional representation of different patrilines within colonies was found, and this remained constant in two consecutive samples of offspring. Dissections showed that all examined queens from multiple-queen colonies were mated egg-layers. The mean relatedness value among nestmate workers in polygynous colonies was lower than that for monogynous colonies. No diploid males were detected in a sample of 70 genotyped males. Worker production of males was detected in one queenless colony. We discuss our findings in relation to known patterns of multiple maternity and paternity in other eusocial Hymenoptera. Received: 2 September 1998 / Received in revised form: 3 February 1999 / Accepted: 7 February 1999     

Alpha-male paternity in elephant seals

The aim of this study was to assess paternity of males that dominated mating in harems at northern (Mirounga angustirostris) and southern (M. leonina) elephant seal rookeries using DNA fingerprinting and microsatellite DNA analysis. Southern alpha males had greater reproductive success than most northern alphas at similar-sized harems. Comparison of the relatedness between pups within harems also suggested that fewer males achieved matings in the southern elephant seal population. This was consistent with behavioral observations that suggest greater competition for mates in northern elephant seal harems. Reproductive success was consistent with estimates of mating success in some cases, but lower than expected for some northern elephant seal alpha males. A lower reproductive success than predicted from mating behavior may arise from a variety of factors including sperm competition, male sperm depletion from frequent mating, or reduced fertility. The alternatives are discussed in the context of environmental and historical factors. Received: 17 August 1998 / Received in revised form: 28 March 1999 / Accepted: 30 May 1999     

Parental investment, potential reproductive rates, and mating system in the strawberry dart-poison frog, Dendrobates pumilio

We studied the effect of relative parental investment on potential reproductive rates (PRRs) to explain sex differences in selectivity and competition in the dart-poison frog Dendrobates pumilio. We recorded the reproductive behavior of this species in a Costa Rican lowland rainforest for almost 6 months. Females spent more time on parental care than males, and `time out' estimates suggest that PRRs of males are much higher than than those of females, rendering females the limiting sex in the mating process. Males defended territories that provide suitable calling sites, space for courtship and oviposition, and prevent interference by competitors. Male mating success was highly variable, from 0 to 12 matings, and was significantly correlated with calling activity and average perch height, but was independent of body size and weight. Estimates of opportunity for sexual selection and variation in male mating success are given. The mating system is polygamous: males and females mated several times with different mates. Females were more selective than males and may sample males between matings. The discrepancy in PRRs between the sexes due to differences in parental investment and the prolonged breeding season is sufficient to explain the observed mating pattern i.e., selective females, high variance in male mating success, and the considerable opportunity for sexual selection. Received: 9 June 1998 / Received in revised form: 27 March 1999 / Accepted: 3 April 1999     

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     

Scramble competition selects for greater tailfin size in male red-spotted newts (Amphibia: Salamandridae)

Darwin predicted that scramble competition for access to reproductive females would result in sexual dimorphism of locomotory structures, but direct evidence for this is extremely rare. I examined the relationship between variation in tailfin size and mating success in a field and laboratory study of red-spotted newts, Notophthalmus viridescens. Over three breeding seasons, male tailfin size was positively correlated with variation in male amplexus frequency, and indirectly correlated with male insemination frequency. In a laboratory study, I confirmed that males' ability to capture females is affected by variation in tailfin size. This is the first study to show that naturally occurring variation in male locomotory structures affects male mating success. It corroborates the prediction that scramble competition leads to sexual selection on locomotory structures and, potentially, to dimorphism in these structures. Received: 16 April 1999 / Received in revised form: 16 May 1999 / Accepted: 12 June 1999     

Female choice in the opportunistic mating of wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale

For female chimpanzees (Pan troglodytes schweinfurthii) in the Mahale Mountains National Park, Tanzania, the most common mating pattern is opportunistic. In such opportunistic matings, females copulated promiscuously but not randomly. This study describes female mate choice during 1-year observation of six females who exhibited regular genital-swelling cycles. During the study period, 169 opportunistic matings and four restrictive matings were recorded over the course of 51 days. As female estrus progressed, mating frequency and the number of adult male mating partners increased, although the number of potential mating partners did not change. Criteria of female choice examined were the direction and consent/rejection of courtship, proximity maintenance, and female grooming. Adult-male courtships were successful more often than those of adolescent males. During the earlier phase of estrus, females copulated rather promiscuously with many males. But during the later phase of estrus when the likelihood of conception is expected to be highest, they copulated repeatedly with high-ranking adult males. There was a positive correlation between female grooming frequency and mating frequency when the likelihood of conception was greatest. Female chimpanzees are thought to choose high-ranking males as fathers of their offspring. Moreover, female chimpanzees may adopt one or both of two mating strategies, i.e., a many-male strategy and a best-male strategy. Received: 23 November 1998 / Received in revised form: 12 April 1999 / Accepted: 26 April 1999     

Male genital traits and mating interval affect male fertilization success in the water strider Gerris lacustris

Parker's seminal work brought attention to the possibility of postmating sexual selection by non-random fertilization success. Mechanisms for these processes are still only partly understood and there is clearly a need for more studies of intraspecific variation in sperm precedence. Here, we report results from an experimental study of the variation in fertilization success between males of the water strider Gerris lacustris. Genital morphology, male body size, and copulation duration were examined as possible correlates of paternity. The significance of guarding duration was also analysed. Only male genital morphology was correlated to fertilization success. This is one of the first studies showing a relationship between male genital traits and fertilization success, supporting the view that sexual selection may be responsible for the rapid and divergent evolution of genital structures in animals with internal fertilization. The fertilization success of last males varied considerably after double matings with a short mating interval (10 min). Last-male priority ranged from 0 to 100% and usually one of the males involved fertilized almost all the eggs. After double matings with a short mating interval, the proportion of eggs fertilized by the last male averaged 0.68 and was greater than 0.5. In contrast, the average fertilization success was biased towards the first male when the matings were more spread out over time (24 h). These results do not support earlier suggestions of a widespread last-male sperm priority in water striders. Received: 28 July 1998 / Received in revised form: 15 March 1999 / Accepted: 28 March 1999     

Positive association of queen number and queen-mating frequency Myrmica ants: a challenge to the genetic-variability hypotheses

Detailed knowledge of the mating system in specific social insect populations is essential for testing general evolutionary hypotheses of multiple paternity in eusocial Hymenoptera. We have studied the mating frequency of queens in a polygynous population of the red ant Myrmica sulcinodis. Genetic mother-offspring analysis showed that double mating occurred at a considerable frequency, but that the effective number of queen-mates remained close to one. After quantifying the effects of multiple maternity (polygyny) and multiple paternity (polyandry) on the genetic diversity of workers, we conclude that multiple paternity in M. sulcinodis did not evolve as an adaptation to increase genetic variation within colonies. Contrary to the predictions from `genetic variability' hypotheses, we found a positive correlation between colony-specific queen number and the average number of mates per queen. Such positive association of queen number and frequency of multiple mating was also found after analysing comparative data across six species of Myrmica ants. These results suggest that resticted dispersal of young queens may be a common factor promoting both polygyny and polyandry at the same time, and that moderate degrees of multiple mating may be an unselected consequence of (1) mating at low cost when mating occurs close to the nest and (2) mating in swarms with a highly male biased operational sex ratio. Future comparative tests of genetic-variability hypotheses should therefore not include species with such evolutionary derived mating system characteristics. Received: 30 April 1998 / Accepted after revision: 19 August 1998     

Male care and mating effort among Hadza foragers

Paternal care figures prominently in many scenarios of human evolution. Recently, however, such scenarios have been challenged on two scores. First, the level of male contribution may be insignificant. Second, male care may be provided as a form of mating effort, rather than parenting effort. In theory, since men can enhance their Darwinian fitness both by providing care to their own offspring if this raises offspring fitness and by pursuing additional mates if this leads to additional offspring, men should respond to payoffs from both mating and parenting effort. If men respond to payoffs from parenting effort, paternity ought to make a difference. And if men respond to payoffs from mating effort, mating opportunities ought to make a difference. I analyzed the impact of these two factors on variation in male care among the Hadza, a foraging society in Tanzania. Two predictions were tested: (1) biological children will receive more care than stepchildren, and (2) men will provide less care to their biological children as their mating opportunities increase. Both predictions were supported. These results suggest men provide care, in part, as parenting effort, and that they trade off parenting effort for mating effort when they have greater mating opportunities. Received: 21 January 1998 / Received in revised form: 24 January 1999 / Accepted: 1 February 1999     

Extended family structure in the ant Formica paralugubris: the role of the breeding system

In populations of various ant species, many queens reproduce in the same nest (polygyny), and colony boundaries appear to be absent with individuals able to move freely between nests (unicoloniality). Such societies depart strongly from a simple family structure and pose a potential challenge to kin selection theory, because high queen number coupled with unrestricted gene flow among nests should result in levels of relatedness among nestmates close to zero. This study investigated the breeding system and genetic structure of a highly polygynous and largely unicolonial population of the wood ant Formica paralugubris. A microsatellite analysis revealed that nestmate workers, reproductive queens and reproductive males (the queens' mates) are all equally related to each other, with relatedness estimates centring around 0.14. This suggests that most of the queens and males reproducing in the study population had mated within or close to their natal nest, and that the queens did not disperse far after mating. We developed a theoretical model to investigate how the breeding system affects the relatedness structure of polygynous colonies. By combining the model and our empirical data, it was estimated that about 99.8% of the reproducing queens and males originated from within the nest, or from a nearby nest. This high rate of local mating and the rarity of long-distance dispersal maintain significant relatedness among nestmates, and contrast with the common view that unicoloniality is coupled with unrestricted gene flow among nests. Received: 8 February 1999 / Received in revised form: 15 June 1999 / Accepted: 19 June 1999     

The genetic mating system of a sex-role-reversed pipefish (Syngnathus typhle): a molecular inquiry

In the pipefish Syngnathus typhle as in other species of Syngnathidae, developing embryos are reared on the male's ventral surface. Although much laboratory research has been directed toward understanding sexual selection in this sex-role-reversed species, few studies have addressed the mating behavior of S. typhle in the wild, and none has capitalized upon the power of molecular genetic assays. Here we present the first direct assessment of the genetic mating system of S. typhle in nature. Novel microsatellite loci were cloned and characterized from this species, and employed to assay entire broods from 30 pregnant, field-captured males. Genetic analysis of 1340 embryos revealed that 1–6 females (mean = 3.1) contributed to each brooded clutch, the highest rate of multiple maternity yet documented in any pipefish. Evidence of multiple mating by females was also detected. Thus, this population of S. typhle displays a polygynandrous mating system, a finding consistent with previous field and laboratory observations. Our results, considered together with similar studies of other syngnathid species, provide preliminary support for the hypothesis that the genetic mating system is related to the evolution of sexual dimorphism in the fish family Syngnathidae. Received: 19 January 1999 / Received in revised form: 15 April 1999 / Accepted: 9 May 1999     

Frequency and timing of extrapair fertilisation in the polyandrous red phalarope (Phalaropus fulicarius)

In sequentially polyandrous bird species, where females mate with different males in succession during a single breeding season, sperm stored by females can occasionally lead to extrapair fertilisations (EPFs) in clutches cared for by the second and subsequent males. Thus, we predicted that in red phalaropes (Phalaropus fulicarius) – a sex-role-reversed, sequentially polyandrous, arctic breeding shorebird – EPFs would occur more frequently in clutches laid later in the breeding season. We used multilocus DNA profiling to examine the frequency and timing of EPFs in a population of red phalaropes breeding in the Canadian high arctic. Using a technique to determine parentage without maternal DNA, we inferred that 6 of 70 chicks in 18 broods resulted from EPFs – one extrapair chick in each of 6 broods. These results were supported by a further analysis using microsatellite DNA. As predicted, broods containing EPFs hatched from clutches laid significantly later in the season than did broods containing no EPFs. The difference in median hatch dates between broods with and without EPFs was 9.0 days, or 38% of the entire egg-laying period in that season. For the whole breeding season, we estimated that 6.5% of chicks were sired by extrapair males, which is similar to extrapair paternity estimates for other sex-role-reversed birds, but relatively low compared to the majority of socially monogamous species studied so far. Received: 24 August 1998 / Received in revised form: 18 January 1999 / Accepted: 24 January 1999     

The cost of sexual coercion and heterospecific sexual harassment on the fecundity of a host-specific, seed-eating insect (Neacoryphus bicrucis)

Two species of seed-eating true bugs, Neacoryphus bicrucis (Heteroptera: Lygaeidae) and Margus obscurator (Heteroptera: Coreidae) co-occur on ragwort, Senecio tomentosus, in southern Georgia, USA. Males of both species sometimes engage in chases and protracted grappling with females that flee initial mountings. Sometimes genital coupling occurs while the wriggling female is restrained in the male's grasp. Chases, grappling, and mounting attempts are misdirected toward heterospecific females, heterospecific males, or conspecific males. In a laboratory study, confinement of mated N. bicrucis females with either conspecific or heterospecific males reduced fecundity by approximately one-half relative to mated females confined only with other females. Perhaps as a consequence of this, N. bicrucis females frequently leave areas of high host plant density, where they prefer to oviposit, when males are abundant. The abundance of each species is positively correlated with host plant density but the two species rarely occur together on the same plants. This may be an effect of heterospecific courtship which induces the flight of N. bicrucis more than the flight of M. obscurator. The laboratory results suggest that copulations following chases and grappling represent sexual harassment, not a mechanism of active female choice for a vigorous mate. As sexual harassment imposes high fitness costs that favor abandonment of host plants, it may, when misdirected, incidentally limit habitat use by ecologically similar species. Received: 3 October 1998 / Received in revised form: 21 January 1999 / Accepted: 14 February 1999     

Polyandry and enhanced reproductive success in the harlequin-beetle-riding pseudoscorpion

The growing molecular evidence that females of many species mate with several males calls for a critical reassessment of the selective forces which act to shape female mating tactics. In natural populations of the harlequin-beetle-riding pseudoscorpion, Cordylochernes scorpioides, females are polyandrous and typically produce mixed-paternity broods. Laboratory behavioral analyses and breeding experiments indicate that polyandry in this pseudoscorpion is an active strategy which increases female reproductive success. Females restricted to mating with a single male experienced a higher rate of embryo failure and produced significantly fewer offspring than either females mated to more than one male in the laboratory or females naturally inseminated in the field. Forced copulation, insufficient sperm from a single mating, male nutrient donations and variation in inherent male genetic quality cannot explain the greater number of nymphs hatched by polyandrous females in this study. Evidence suggests that, by mating with several males, C. scorpioides females may exploit postcopulatory mechanisms for reducing the risk and/or cost of embryo failure resulting from fertilization by genetically incompatible sperm. Received: 5 May 1996 / Accepted after revision: 16 October 1996     

Determinants of male mating success in the red bishop (Euplectes orix)

We studied sexual selection in the red bishop, Euplectes orix, a colonial, polygynous weaverbird widely distributed over sub-Saharan Africa. Male reproductive success measured in terms of the number of nests accepted by females and the number of eggs and nestlings in all the nests on a male's territory varied considerably. The standardized variance (variance/mean²) in male reproductive success ranged from 0.505 to 1.737 in different years, indicating a high potential for sexual selection in this species. An analysis of genetic parentage for 432 nestlings by non-radioactive, multilocus DNA fingerprinting confirmed that male reproductive success (number of young sired on the territory) in this species can be reliably estimated by the measures introduced above. In all 4 study years there was a strong positive correlation between male mating success and the total number of nests that males built in their territories. The number of nests built can be partitioned into the number of weeks a male held a territory and his nest-building performance. Both factors exert a significant positive effect on male mating success and in combination explained between 53.3 and 86.3% of the variation in male reproductive success. Male morphological characters were found to be of no importance. Males that established a territory in the following season built more nests and held their territories for longer than males that did not establish a territory in the following season, suggesting that these measures might be indicators of male condition and quality. Male nest-building performance (number of nests built per week) seems to be unrelated to male condition or quality. Received: 8 January 1999 / Received in revised form: 7 June 1999 / Accepted: 13 June 1999     

Behavioral aspects of sperm competition in cuttlefish, Sepia officinalis (Sepioidea: Cephalopoda)

Sexual selection studies in cephalopods indicate that sperm competition is a central feature of their mating systems, yet this has not been studied experimentally in any detail. In 1998 we staged 20 matings of the cuttlefish, Sepia officinalis L., in the laboratory. Males rapidly initiated mating in the “head-to-head” position, with no apparent courtship. Mating lasted an average of 10 min (range 7 to 14 min). For the first 6 min (on average 63% of the mating duration), the male flushed strong jets of water directly at the female's buccal membrane, which sometimes resulted in the expulsion of parts of spermatangia placed there in recent matings. Then, in a single discrete movement that lasted an average of only 14 s, the male's modified fourth left arm – the hectocotylus – wrapped around a single large bundle of spermatophores (ca. 150 to 300) and transferred them to the female's buccal membrane. For the remainder of the mating (average 3 min, range 1.5 to 5.0 min), the hectocotylus repeatedly broke the spermatophores open, and manipulated them, so that sperm were released and many spermatangia were attached along the ventral buccal membrane, near the paired seminal receptacles. Approximately 140 spermatangia were attached in rows 3 to 5 deep around the ventral buccal membrane in a single mating; the rest were usually discarded during mating. Histology revealed that each of the seminal receptacles consists of a series of sperm storage bulbs connected by a central duct, which leads to a single pore at the surface of the buccal membrane. Baseline data on sperm motility were obtained, but the mechanism by which sperm enter the seminal receptacle remains unknown. Females seemed to initiate termination of mating, then males guarded their mates temporarily. These results, combined with other recent laboratory experiments, provide evidence that sperm competition may be a major feature of the mating system of S. officinalis. Received: 4 January 1999 / Accepted: 18 May 1999     

Mating patterns and reproductive success in the bushy-tailed woodrat (Neotoma cinerea), as revealed by DNA fingerprinting

The mating patterns and reproductive success of the bushy-tailed woodrat (Neotoma cinerea) were investigated over a 3-year period (1992–1994) using DNA fingerprinting. Paternity was determined by genetic analysis of 58 juveniles of known maternity from 35 litters. Analysis of DNA fingerprints revealed that all offspring within a litter were fathered by a single male; the statistical probability of detecting multiple males mating with a female was high, indicating that multiple paternity would have been detected had it occurred. However, individual males did not father more than one litter from a given female either within or between years. At least 75% of females and 57% of males successfully produced offspring each year. The finding that all littermates are first-order relatives may contribute to the high level of female cooperation in this species. Received: 28 May 1997 / Accepted after revision: 22 March 1998     

Sperm precedence and sperm storage in multiply mated red flour beetles

In insects, the last male to mate with a female often gains access to a disproportionate number of subsequent fertilizations. This study examined last-male sperm precedence patterns in doubly and triply mated Tribolium castaneum females. Sperm storage processes were investigated by measuring the quantity of sperm stored within the female spermatheca following single, double, and triple matings. Both doubly mated and triply mated females exhibited high last-male sperm precedence for progeny produced during the first 48 h following the last mating, with females in both groups exhibiting parallel declines in sperm precedence 1 and 2 weeks later. The number of sperm stored by females increased by 33% between singly mated and doubly mated females, indicating that the spermatheca is filled to only two-thirds capacity following insemination by the first male. Based on the proportion of stored sperm from first and second matings, we tested predictions about sperm precedence values based on models of random sperm mixing. High initial last-male sperm precedence strongly supports stratification of last-male sperm. By 1–2 weeks after double matings, sperm precedence declined to levels indistinguishable from values expected under random mixing. These results provide insight into mechanisms of sperm storage and utilization in this species. Received: 20 August 1997 / Accepted after revision: 24 May 1998     

Reduced take-off ability in robins (Erithacus rubecula) due to migratory fuel load

Recent studies have shown that large fuel loads in small birds impair flying ability. This is the first study to show how migratory fuel load affects flying ability, such as velocity and height gained at take-off in a predator escape situation, in a medium-distance migrant, and whether they adjust their take-off according to predator attack angle. First-year robins (Erithacus rubecula) were subjected to simulated attacks from a model merlin (Falco columbarius), and take-off velocity and angle were analysed. Robins with a wing load of 0.19 g cm⁻² took off at a 39% lower angle than robins with a wing load of 0.13 g cm⁻², while velocity remained unaffected. The robins did not adjust their angle of ascent in accordance with the predator's angle of attack. Since many predators rely on surprise attacks, a difference in flight ability due to varying fuel loads found in migrating robins can be important for birds' chances of survival when actually attacked. Received: 28 October 1998 / Received in revised form: 12 January 1999 / Accepted: 30 January 1999     

Oligogyny by unrelated queens in the carpenter ant, Camponotus ligniperdus

Multilocus DNA fingerprinting and microsatellite analysis were used to determine the number of queens and their mating frequencies in colonies of the carpenter ant, Camponotus ligniperdus (Hymenoptera: Formicidae). Only 1 of 61 analyzed queens was found to be double-mated and the population-wide effective mating frequency was therefore 1.02. In the studied population, 8 of 21 mature field colonies (38%) contained worker, male, or virgin queen genotypes which were not compatible with presumed monogyny and therefore suggested oligogyny, i.e., the cooccurrence of several mutually intolerant queens within one colony. Estimated queen numbers in oligogynous colonies ranged between two and five. According to the results of the genetic analysis, most of the queens coexisting in oligogynous colonies were not closely related. Pleometrosis is very rare and queenless colonies adopt mated queens both in the laboratory and field. Therefore, the most plausible explanation for the origin of oligogynous colonies in C. ligniperdus is the adoption of unrelated queens by orphaned mature colonies. The coexistence of unrelated, but mutually intolerant queens in C. ligniperdus colonies demonstrates that oligogyny should be considered as a phenomenon distinct from polygyny. Received: 18 December 1997 / Accepted after revision: 20 June 1998