On the mating system of the cooperatively breeding saddle-backed tamarin (Saguinus fuscicollis)

Summary This paper reports on 5 years of observatiors of individually marked saddle-backed tamarins (Saguinus fuscicollis, Callitrichidae). Although callitrichids have long been presumed to have a monogamous social system, this study shows that the breeding structure of saddle-back tamarin groups is highly variable. Groups most commonly include two or more adult males and a single reproductive female, but occasionally contain only a single pair of adults, or less often, two reproductively active females and one or more males. Data on group compositions, group formations, intergroup movements and copulations show that the social and mating systems of this species are more flexible than those of any other non-human primate yet studied. Infants (usually twins) were cared for by all group members. There were two classes of helpers: young, nonreproductive individuals who helped to care for full or half siblings, and cooperatively polyandrous males who cared for infants whom they may have fathered. The observations suggest that non-reproductive helpers may benefit from their helping behavior through a combination of inclusive fitness gains, reciprocal altruism, and the value of gaining experience at parental care.     

Social relationships in a cooperatively polyandrous group of tamarins (Saguinus fuscicollis)

Summary This paper presents detailed data on the social relationships among the adults, and between the adults and young, of a cooperatively polyandrous saddle-back tamarin (Saguinus fusciollis; Callitrichidae) group studied for one year. Some data are also presented from groups studied in other years. Adult males in the study groups gave more grooming than they received, while the opposite was true for females (e.g. Fig. 1). The two polyandrous males in the main study group were very rarely aggressive to each other, rarely tried to disrupt each others' copulations, groomed each other, and occasionally shared food, suggesting that their relationship was more affiliative than agonistic. Data on grooming (Fig. 2), spatial relationships, and the initiation of copulations suggest that the males of this group, may have been somewhat more responsible than the female for the maintenance of male-female relationships. Both males and females performed all forms of parental care except lactation. In the main study group each of the males groomed the offspring and remained in close proximity to them more than did the female (Figs.3 and 4). These data are compared with existing data on social relationships in bird species that exhibit cooperative polyandry.     

Sex allocation and paternity in a cooperatively breeding passerine: evidence for the male attractiveness hypothesis?

Sex allocation theory predicts that female birds with high-quality mates will benefit from producing more sons, since sons will inherit their father’s superior traits and enjoy a great reproductive success, whereas females with low-quality mates will benefit from producing more daughters, since the variance in reproductive success among daughters is typically lower. The male attractiveness hypothesis may apply to extra-pair paternity (EPP) because socially monogamous females routinely mate with higher quality males outside the pair bond. We test these predictions using the Tibetan ground tit (Pseudopodoces humilis), a sexually monomorphic, socially monogamous, facultatively cooperative breeder. There was greater variation in actual reproductive success among males than females due to EPP. An excess of sons was detected for bi-parental (i.e., non-cooperative) broods wherein EPP was mainly sired by bi-parental males. The pattern was attributed to male-biased sex ratios produced for both EPP and within-pair offspring within the same broods. The reason for the latter case might be a random allocation of more offspring to sons by the potentially EPP-exposed females that have an inability to control fertilization by specific males. In cooperative broods where EPP mostly resulted from within-group helpers of presumed low-quality, as indicated by their failure in acquiring a social mate, there was a non-significant tendency for EPP offspring to be daughters and for within-pair offspring in the same broods to be unbiased. These results support the EPP-related male attractiveness hypothesis especially in terms of the overproduction of sons. Offspring produced through quasi-parasitism was unbiased towards either sex, suggesting a weak female choiceness with respect to the quality of host males.     

Male care of infants in a siamang (Symphalangus syndactylus) population including socially monogamous and polyandrous groups

While male parental care is uncommon in mammals, siamang (Symphalangus syndactylus) males provide care for infants in the form of infant carrying. I collected behavioral data from a cohort of five wild siamang infants from early infancy until age 15–24 months to identify factors affecting male care and to assess the consequences of male care for males, females, and infants in a population including socially monogamous groups and polyandrous groups. There was substantial variation in male caring behavior. All males in polyandrous groups provided care for infants, but males in socially monogamous groups provided substantially more care than males in polyandrous groups, even when the combined effort of all males in a group was considered. These results suggest that polyandry in siamangs is unlikely to be promoted by the need for “helpers.” Infants receiving more care from males did not receive more care overall because females compensated for increases in male care by reducing their own caring effort. There was no significant relationship between indicators of male–female social bond strength and male time spent carrying infants, and the onset of male care was not associated with a change in copulation rates. Females providing more care for infants had significantly longer interbirth intervals. Male care may reduce the energetic costs of reproduction for females, permitting higher female reproductive rates.     

Fallow deer polyandry is related to fertilization insurance

Polyandry is widespread, but its adaptive significance is not fully understood. The hypotheses used to explain its persistence have rarely been tested in the wild and particularly for large, long-lived mammals. We investigated polyandry in fallow deer, using female mating and reproduction data gathered over 10 years. Females of this species produce a single offspring (monotocous) and can live to 23 years old. Overall, polyandry was evident in 12 % of females and the long-term, consistent proportion of polyandrous females observed, suggests that monandry and polyandry represent alternative mating strategies. Females were more likely to be polyandrous when their first mate had previously achieved high numbers of matings during the rut or was relatively old. However, polyandry was not related to the following factors: female age, the stage of the rut, the dominance ranks of mates, or the number of daily matings achieved by males. Polyandrous and monandrous multiple-mating females were not more likely than single-mating females to be observed with an offspring during the following year, and there were no significant differences in offspring size between these females. These results provide support for a fertility insurance hypothesis, with females remating if fertilization from the first mating was uncertain due to possible sperm depletion. The potential for different female mating strategies among large, polygynous mammals has generally been overlooked. Our findings highlight the complexity of female reproductive strategies and the possible trade-offs between fertilization success, preferences for high-quality males, and potential costs of polyandry, particularly for monotocous species.     

Mating system and mating success of the desert spider Agelenopsis aperta

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

The benefits of multiple mating to female seaweed flies, Coelopa frigida (Diptera: Coelpidae)

Female seaweed flies, Coelopa frigida, have the potential to benefit from mating more than once. Single matings result in low fertility so females may benefit directly from multiple copulations by sperm replenishment. A chromosomal inversion associated with larval fitness, with heterokaryotypic larvae having higher viability than homokaryotypes, means that polyandrous homokaryotypic females have a higher probability of producing genetically fit offspring than monandrous homokaryotypic females. We allowed females to mate only once, repeatedly four times to the same male, or polyandrously four times to four different males. Multiply mated and polyandrous females laid more eggs and produced more offspring than singly mated and monandrous females, respectively. Polyandrous females laid more eggs, had higher egg-to-adult survival rates and produced more offspring than repeatedly mated females. Fertility rates did not differ between treatments. The observed fitness patterns therefore resulted from increased oviposition through multiple mating per se, and a further increase in oviposition coupled with higher egg-to-adult offspring survival benefits to polyandry. Daily monitoring of individual females over their entire life spans showed that multiple copulations induced early oviposition, with polyandrous females ovipositing earlier than repeatedly mated females. Singly mated and polyandrous females incurred a longevity cost independent of egg production, whereas repeatedly mated females did not. This suggests that repeatedly mating with the same male may counteract a general cost of mating. Longevity, however, was not correlated with overall female fitness. Our data are discussed in the overall context of the seaweed fly mating system.Communicated by G. Wilkinson     

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     

Polyandrous female butterflies forage for matings

Butterfly mating systems exhibit great variation and range from strict monandry to strong polyandry. During mating males transfer ejaculates containing both sperm and accessory substances to females. In the polyandrous green-veined white butterfly, Pieris napi (Lepidoptera, Pieridae) these ejaculates average 15% of male body mass, but can represent up to 23% of body mass for individual males. Hence, mating is costly to males, and recently mated males increase copula duration but decrease ejaculate mass transferred to females. Substances transferred to females during mating are later incorporated into female soma and reproductive tissues, and multiply mated female butterflies have higher lifetime fecundity, lay proportionately larger eggs, and live longer compared to once mated females. Here we report that females of P. napi allowed to mate at liberty with recently mated males only (i.e. males that delivered a small ejaculate) increased their lifetime number of matings compared to females allowed to mate with virgin males only (i.e. males that delivered large ejaculates), the former group mating on average 5.1 times (range 2–10) and the latter group mating on average 2.8 times (range 1–4). The lifetime fecundity of the two groups of females did not differ significantly. Because nutrient donation from males is essential for females to realize their potential fecundity, we conclude that females of the polyandrous green-veined white actively forage for matings.     

Indirect genetic benefits of polyandry in a spider with direct costs of mating

The search for the evolutionary explanation of polyandry is increasingly focused on direct and indirect selection on female resistance. In a polyandrous spider Stegodyphus lineatus, males do not provide material benefits and females are resistant to remating. Nevertheless, polyandrous females may obtain indirect genetic benefits that offset the costs associated with multiple mating. We manipulated the opportunity for females to select between different partners and examined the effect of female mating history (mated once, mated twice, or rejected the second male) on offspring body mass, size, condition, and survival under high- and low-food rearing regimens. We found that multiple mating, not female choice, results in increased female offspring body mass and condition. However, these effects were present only in low-food regimen. We did not find any effects of female mating history on male offspring variables. Thus, the benefits of polyandry depend not only on sex, but also on offspring environment. Furthermore, the observed patterns suggest that indirect genetic benefits cannot explain the evolution of female resistance in this system.     

Sequential polyandry by brood desertion increases female fitness in a bird with obligatory bi-parental care

Parental care may be costly to parents because it decreases resources allocated to self-maintenance and may thus reduce survival and future reproductive success. An inter-sexual conflict may exist in animals with obligatory bi-parental care, such as birds of prey, in which females incubate and brood, whereas males provision food for their families. We analysed 29 years of data (1981–2009) from a study population of Tengmalm’s owls Aegolius funereus in western Finland to examine the occurrence and timing of brood desertion and sequential polyandry, and recorded a total of 1,123 monogamous and 12 polyandrous females. These data were supplemented with the 29-year nationwide Finnish ringing data, which included 11,590 monogamous and 20 polyandrous females. The 12 polyandrous females started egg-laying in their two nests at intervals of 54–68 days (mean 60 days), thus deserting their first broods when the age of oldest young averaged 21 days. Thirty-two polyandrous females re-mated and raised a second brood at a median distance of 4.5 km (range 1–196 km). These females produced 79% more eggs, 93% more hatchlings and 73% more fledglings than did females that laid simultaneously but remained monogamous. Our results show that not only males, but also females of altricial species with bi-parental care can increase their fitness by deserting their first brood when it will be cared for by the males. Earlier studies have shown that male owls can increase their lifetime reproductive success by simultaneous polygyny, and we suggest that an inter-sexual “tug-of-war” over bi-parental care exists in Tengmalm’s owls.     

Social monogamy and the threat of infanticide in larger mammals

The evolution of social monogamy in larger mammals is difficult to explain because males usually do not invest much in direct offspring care and might achieve greater fitness by deserting a pregnant female to reproduce with additional females elsewhere. It has been hypothesized that socially monogamous males remain with the female year-round to protect their offspring from infanticide by new immigrant males. We investigated this idea by analyzing all cases of infant loss in a wild population of white-handed gibbons (Hylobates lar; Primates), in which most groups were socially monogamous and some polyandrous (137.5 group years). We examined the influence of (a) male intruder pressure on male immigration rates and (b) the presence of a new male in the group on infant loss. We found no relation between intruder pressure and male immigration rates. Infant loss was lowest (4.5%) for stable monogamy (probable father stayed from conception through infancy) and intermediate (25.0%; p = 0.166) for stable polyandry. If a new male immigrated after conception, however, the infant was lost in all cases (p < 0.01) independent of the presumed father’s presence. Overall, 83.3% of infant losses were associated with the presence of a presumably unrelated male. Although the sample size is small, our results provide the first true support for the idea that the risk of infanticide is an important factor in the evolution of social monogamy in larger mammals.     

Seasonal variation in male-female competition,cooperation and selfish hoarding in a monogamous songbird

Both cooperation and conflict between the sexes are commonplace in monogamous mating systems. However, little is known about how cooperation and competition varies seasonally in monogamous species that maintain permanent territories. We presented territorial pairs of male and female New Zealand robins (Petroica australis) with a large supply of insect prey at monthly intervals for 2 years. Behavioural observations after food presentation were then made to quantify seasonal and sexual differences in aggressive interactions over prey, prey acquisition rates, mate provisioning, offspring provisioning, selfish food hoarding and cache retrieval. Data were used to evaluate sex-specific behavioural strategies of mediating competition for food. Results showed that males aggressively excluded females from experimental food sources year-round. Females only accessed food sources when males left them unattended. Consequently, females acquired fewer prey than males. After controlling for differences in prey acquisition, both sexes consumed similar amounts of prey in the non-breeding season. Even though males aggressively excluded females from accessing food sources directly, males fed large amounts of prey to females during the breeding season. Both sexes provisioned young at similar rates. Males cached less prey than females in the breeding season but more prey than females in the non-breeding season. Females showed similar caching intensities year-round. Although males tried to defend their hoards, females frequently retrieved male-made caches. Overall, results showed that although New Zealand robins cooperate to raise offspring during the breeding season, conflict between the sexes occurs year-round. Males and females display different behavioural strategies to gain access to experimental food sources, which appear to lessen male–female competition for food and evenly distribute food resources between the sexes.     

Do male plumage and song characteristics influence female off-territory forays and paternity in the hooded warbler?

Extra-pair fertilizations are common in many socially monogamous species, and paternity studies have indicated that females may use male vocal performance and plumage ornaments as cues to assess male quality. Female off-territory forays may represent a key component of female choice and male extra-pair mating success, and female foray behaviour is expected to be strongly influenced by indictors of male quality. In this study, we examined how male song and ornamentation affect how often females left their territories, which males they visited and extra-pair paternity in a socially monogamous passerine, the hooded warbler (Wilsonia citrina). We radiotracked 17 females during the fertile period and quantified male vocal performance (song output and rate) and plumage characteristics (size of the black melanin hood and colour of the black hood, yellow cheeks and breast areas). We obtained blood samples and determined paternity at 35 nests including those of 14 females that we radiotracked. Eleven (65%) of the 17 females forayed off-territory, whilst fertile and female foray rate was positively correlated with the number of extra-pair young in the nest. Females that left their territories more frequently were paired with males that sang at a low rate. In addition, extra-pair mates had higher song rates than the social mates they cuckolded (5.3 songs/min vs. 4.4 songs/min). Female off-territory forays or extra-pair paternity were not significantly related to male plumage characteristics. Our results indicate that a high song rate influences both the foray behaviour of a male’s social mate and the likelihood that he will sire extra-pair offspring with neighbouring females.     

Female benefit,male risk: Polyandry in the true armyworm Pseudaletia unipuncta

In Lepidoptera polyandry is common and females may increase their lifetime reproductive output through repeated matings if they acquire essential resources from male ejaculates. However, the paternity of males mating with previously-mated females is far from assured unless sperm precedence is absolute. In this study on the polyandrous armyworm, Pseudaletia unipuncta, we used two strains of male (the black-eyed wild type and a red-eyed homozygous, recessive mutant), mated with red-eyed females, to determine (i) whether male investment has any impact on female reproductive output, and (ii) if females do benefit from multiple matings, to what extent males fertilize the eggs to which they contributed. Multiple mating resulted in a significant increase in both the fecundity and longevity of females. However, the degree of sperm precedence (those eggs fertilized by the second male) varied from 0–100%, but was not affected by either male size or age, or by the duration of copulation. In cases where sperm precedence was <50% (x = 12%) females produced significantly more eggs (1384 versus 940) prior to the second mating than females where sperm precedence was >50% (x = 89%), indicating that the quality of the first mating influenced the fertilization success of the female's second mate.     

Male butterfly investment in successive ejaculates in relation to mating system

In Lepidoptera, female mating systems range from strict monandry to strong polyandry. Males transfer an ejaculate during copulation that contains both sperm and accessory gland substances. In butterflies the male ejaculate has at least three effects: it (1) contains sperm that can fertilize the eggs of the male’s mating partner, (2) influences the refractory period of the mated female, and (3) contains nutrients that can be used by the female to increase her reproductive output. A number of recent studies have shown that males in polyandrous mating systems are endowed with adaptations to increase mating capabilities. Relative to males in more monandrous species they transfer larger first ejaculates which contain relatively more protein, and allocate proportionally more resources to reproduction. The objective of this study was to compare male reproductive investment in successive ejaculates, in terms of both mass and quality, to determine if males of polyandrous species are capable of maintaining the production of larger and more nutritious ejaculates than males of more monandrous species. We used three species of pierid butterfly, with mating systems ranging from relative monandry to polyandry. The degree of polyandry had a substantial effect on the reproductive performance of males. The cumulative protein content of ejaculates increased with the degree of polyandry. Only males of the most polyandrous species, Pieris rapae, produced three successive ejaculates of similar mass and protein content. In the relatively monandrous species, Aporia crataegi and P. brassicae, males in subsequent matings never produced another ejaculate as large as that transferred by males mating for the first time, although the protein content (mg) of ejaculates did not differ in second and third ejaculates. Moreover, the ability to remate varied with the degree of polyandry. Given the opportunity to remate, the majority of P. rapae males mated three times, whereas relatively few A. crataegi and P. brassicae males were able to perform three matings. These results suggest that male capacity to produce large, nutritious ejaculates is limited in relatively monandrous species. In this study only males belonging to the most polyandrous species had the ability to recuperate quickly from a mating event and remate. Our results suggest that males in polyandrous systems are better adapted to mating more than once. Received: 3 November 1995/Accepted after revision: 13 July 1996     

Mass and production rate of ejaculates in relation to monandry/polyandry in butterflies

Summary The mating system maintained in a species has a strong effect on the degree of sperm competition, and certainty of paternity should accordingly influence the optimal sperm content, nutrient content, and mass of the ejaculate. We investigated how ejaculate mass relates to the degree of polyandry in 20 species of butterflies belonging to the families Pieridae and Satyridae. We found that the degree of polyandry has a substantial effect on the reproductive performance of males. The allometric line between ejaculate mass and male body mass has a higher elevation in the pierids compared to the satyrids. The mean number of matings performed by the pierid species is also higher compared to the mean of the satyrids. Thus, the relative ejaculate mass is larger in the family in which polyandry is more pronounced. A within family effect of degree of polyandry on relative ejaculate mass was also detected in the pierids. Since males of polyandrous species on average mate more often than males of monandrous species, they should be expected to have a higher capacity for producing many ejaculates. We investigated how this capacity was influenced by the degree of polyandry, by allowing males of seven different species (Danaus plexippus, Lasiommata megera, Papilio machaon, Pararge aegeria, Pieris napi, Pieris rapae, and Polygonia c-album) to mate twice, with different time intervals between matings. The results showed that not only is the mass of the ejaculate greater in more polyandrous species, but also the rate at which males are able to produce sperm and accessory substances is greater. Hence our data indicate that sperm competition is important for explaining variation in ejaculate mass in butterflies.     

Multiple mating in the ant Acromyrmex versicolor: a case of female control

In eusocial insects, polyandrous mating has the potential to reduce genetic relatedness of individuals within a colony, which may have a profound effect on the stability and social structure of the colony. Here we present evidence that multiple mating is common in both males and females of the desert leaf-cutter ant Acromyrmex versicolor. Females seem to have complete control over the number of matings, and mate on average with three males, even though the sperm transferred in a single copulation is sufficient to fill the spermatheca. To determine whether there is a bias in the representation of sperm from different mates in the spermatheca, females were mated to three or four males in controlled mating experiments and were subsequently allowed to found colonies in the laboratory. Paternity analysis of the offspring by random amplified polymorphic DNA analysis showed that all males that have been mated to a female successfully contributed sperm to the production of her offspring. No significant asymmetry in sperm use was detected, suggesting complete sperm mixing. Different hypotheses to explain polyandrous mating are discussed, and it is argued that the best hypothesis to explain polyandrous mating and complete sperm mixing in A. versicolor is that utilizing genetically diverse sperm confers a selective advantage on females. Received: 14 June 1995/Accepted after revision: 26 November 1995     

No evidence of mate discrimination against males carrying a sex ratio distorter in <Emphasis Type="Italic">Drosophila pseudoobscura</Emphasis>

Selfish genetic elements (SGEs) that spread by manipulating spermatogenesis often have highly deleterious effects on males that carry them. Females that mate with male carriers of SGEs can also suffer significant costs: they receive fewer and poorer-quality sperm, their offspring will inherit the deleterious allele, and the sex ratio of their offspring will be biased towards the more common sex. To counter these costs, females are therefore expected to prefer to mate with males that do not carry sex ratio distorters or other deleterious selfish genetic elements. However, despite the potential costs, there are few examples of female choice against males carrying SGEs. We searched for evidence of a female preference in fruit fly Drosophila pseudoobscura against males carrying a costly meiotic driving X-chromosome Sex Ratio (SR). In a series of five non-competitive mate preference experiments, we find no evidence that females prefer to mate with non-SR males. Our use of five separate experiments, involving more than 800 females, makes it unlikely that this lack of a difference was due to low power or simple chance. We suggest that the lack of female choice against SGE-carrying males may be due to strong selection on SGEs to be indistinguishable from alternative alleles. Furthermore, polyandry, either in direct response to receiving an ejaculate from an SGE-carrying male or carried out indiscriminately when at risk of mating with carriers, may be an alternative response by females to limit the exposure of their offspring to SGEs.     

Do female bank voles (Clethrionomys glareolus) mate multiply to improve on previous mates?

Contrary to classical sexual selection theories, females of many taxa mate with multiple males during one reproductive cycle. In this study, we conducted an experiment on the “trade-up hypothesis”, which proposes that females remate if a subsequently encountered male is potentially superior to previous mates to maximize the genetic quality of their offspring. We presented bank vole females (Clethrionomys glareolus) sequentially with two males of known dominance rank in different orders, i.e., either first subordinate and second dominant, first dominant and second subordinate, or two males that were equal in dominance (high ranking) and observed their mating behavior. We found that 92% of the females mated multiply and did not base their remating decision on male social status. Therefore, polyandry cannot be explained by the “trade-up hypothesis” based on dominance rank in this species. However, we found that dominant males sired significantly more offspring than subordinate males. This varied according to mating order: dominant males sired more offspring when they were second than when they were first. Moreover, litter sizes were significantly smaller when the dominant male was first (smallest relative success of dominant males) compared to litter sizes when mating order was reversed or both males equal in status. Our results suggest that even though multimale mating includes males that are of poorer quality and thus potentially decreases the fitness of offspring, most of a female’s offspring are sired by dominant males. Whether this is due to cryptic female choice, sperm competition, or a combination of both, remains to be tested.