Levels Of Polyandry Research Articles

Mating frequency estimation and its importance for colony abundance analyses in eusocial pollinators: a case study of Bombus impatiens (Hymenoptera: Apidae).

The genus Bombus (bumble bees) includes approximately 265 species, many of which are in decline in North America and Europe. To estimate colony abundance of bumble bees in natural and agricultural habitats, sibship relationships are often reconstructed from genetic data with the assumption that colonies have 1 monandrous queen. However, some species such as the North American common eastern bumble bee (Bombus impatiens Cresson) can display low levels of polyandry, which may bias estimates of colony abundance based on monandrous sibship reconstructions. To accurately quantify rates of polyandry in wild and commercially mated queens of this species, we empirically estimated mating frequencies using a novel statistical model and genotypes from 730 bees. To genotype individuals, we used a highly polymorphic set of microsatellites on colonies established from 20 wild-caught gynes and 10 commercial colonies. We found multiple fathers in 3 of the wild colonies and 3 of the commercial colonies. This resulted in average effective mating frequencies of 1.075 ± 0.18 and 1.154 ± 0.25 for wild and commercial colonies, respectively. These findings agree with previous reports of low rates of polyandry for B. impatiens. Using a large empirical dataset, we demonstrate that assuming monandry for colony abundance estimation in species that violate this assumption results in an overestimation of the number of colonies. Our results emphasize the importance of studying mating frequencies in social species of conservation concern and economic importance for the accuracy of colony abundance estimation and for understanding their ecology and sociobiology.

Mechanisms for polyandry evolution in a complex social bee

Polyandry in social Hymenoptera is associated with reduced within-colony relatedness and increased colony-level ecologic fitness. One explanation for this sees increasing within-nest genetic diversity as a mechanism for improving group task efficiency and colony competitiveness. A queen on her mating flight captures nearly 90% of her breeding population’s allele potential by her tenth effective mating (me ~ 10 males). Under this population allele capture (PAC) model, colony fitness gains track mating number in an asymptotic manner, leveling out after about the tenth mating. A supporting theory we call the genotype composition (GC) model sees genetic novelty at mating levels higher than the me ~ 10 asymptote, the hyperpolyandry zone, resulting from unique genotype compositions whose number are potentially infinite. Colony fitness gains under the GC model will track mating number in a linear manner. We set up field colonies with Apis mellifera queens each instrumentally mated with 1, 2, 4, 8, 16, or 32 males, creating a polyandry gradient bracketing the qualitative divide of me ~ 10, measured tokens of colony level fitness, and collected observation hive data. Our results lead us to conclude that (1) ancestral colony traits fundamental to eusociality (cooperative brood care) respond to mating level changes at or below me ~ 10 in a manner consistent with the PAC model, whereas (2) more derived specialized colony phenotypes (resistance to the non-native parasite Varroa destructor) continue improving with increasing me in a manner consistent with the GC model. By either model, (3) the mechanism for increasing colony fitness is an increase in worker task specialisms and task efficiency.Significance statementPolyandry is a female’s practice of mating with many males, storing their sperm, and using it to produce genetically diverse offspring. In complex social bees, a queen captures nearly 90% of her breeding population’s diversity potential by her tenth mating; however, queens in nature routinely mate with many more than ten males. We tested two models that, together, explain how social bee colonies ecologically benefit from queen mating numbers ranging from 2 to potential infinity. A population allele capture (PAC) model focuses on colony fitness gains at mating numbers at or below 10, and we provide evidence that it was at these polyandry levels that significant gains were made in an ancestral eusocial trait, cooperative brood care. A genotype composition (GC) model focuses on colony fitness gains at higher mating numbers, and we believe these gains are centered around more recently evolved ecologic specialisms such as parasite resistance.

Novel insights into paternity skew in a polyandrous social wasp.

Females of many species are polyandrous. However, polyandry can give rise to conflict among individuals within families. We examined the level of polyandry and paternity skew in the common eastern yellowjacket wasp, Vespula maculifrons, in order to gain a greater understanding of conflict in social insects. We collected 10 colonies of V. maculifrons and genotyped workers and prereproductive queens at highly variable microsatellite markers to assign each to a patriline. Genotypic data revealed evidence of significant paternity skew among patrilines. In addition, we found that patrilines contributed differentially to caste production (worker vs. queen), suggesting an important role for reproductive conflict not previously discovered. We also investigated if patterns of paternity skew and mate number varied over time. However, we found no evidence of changes in levels of polyandry when compared to historical data dating back almost 40years. Finally, we measured a suite of morphological traits in individuals from the most common and least common patrilines in each colony to test if males that showed highly skewed reproductive success also produced offspring that differed in phenotype. Our data revealed weak correlation between paternity skew and morphological phenotype of offspring sired by different males, suggesting no evidence of evolutionary tradeoffs at the level investigated. Overall, this study is the first to report significant paternity and caste-associated skew in V. maculifrons, and to investigate the phenotypic consequences of skew in a social wasp. Our results suggest that polyandry can have important consequences on the genetic and social structure of insect societies.

A putatively new ant species from the Cataglyphis cursor group displays low levels of polyandry with standard sexual reproduction

A putatively new ant species from the Cataglyphis cursor group displays low levels of polyandry with standard sexual reproduction

Evidence of the Genetic Mating System in Viviparity White-Edged Rockfish, <i>Sebastes taczanowskii</i> Steindachner, 1880

Internal fertilization and viviparity are characteristic of some species of the genus Sebastes. Polyandry has also been reported for some species of this genus. We used five microsatellite markers and three main statistical approaches to estimate the level of polyandry in a wild population of white-edged rockfish (Sebastes taczanowskii). In some clutches, we detected multiple paternity. This study is the first record of multiple paternity in white-edged rockfish from the Far East. Polyandry is probably quite a widespread strategy in this species inhabiting the Far Eastern seas, and also an important factor in the regulation of genetic diversity and productivity.

Differential resistance across paternal genotypes of honey bee brood to the pathogenic bacteriumMelissococcus plutonius

AbstractMelissococcus plutoniusis a pathogenic bacterium affecting immature stages of the western honey bee (Apis mellifera) and leads to European foulbrood (EFB) disease. Despite EFB outbreaks increasing in frequency in several countries in recent decades, there is little knowledge on the epidemiology ofM. plutoniusor on the defence mechanisms of honey bees against this pathogen. Mating of honey bee queens with multiple males (polyandry) can be such a mechanism, as it has been shown to be beneficial to colony health and fitness. It is hypothesized that a high level of polyandry was selected for in response to pathogen pressure to maximize the probability that at least some patrilines among nestmates in a colony possess a high degree of resistance to specific pathogens, ultimately protecting colonies against infections. We show thatM. plutoniusinfection provokes differential mortality among patrilines of immature honey bee workers. Such differences indicate a genetic origin of resistance against this pathogen—supporting the polyandry hypothesis—and open up avenues to improve control of EFB disease via selective breeding.

Temporal Analysis of Effective Population Size and Mating System in a Social Wasp

Highly social species are successful because they cooperate in obligately integrated societies. We examined temporal genetic variation in the eusocial wasp Vespula maculifrons to gain a greater understanding of evolution in highly social taxa. First, we wished to test if effective population sizes of eusocial species were relatively low due to the reproductive division of labor that characterizes eusocial taxa. We thus estimated the effective population size of V. maculifrons by examining temporal changes in population allele frequencies. We sampled the genetic composition of a V. maculifrons population at 3 separate timepoints spanning a 13-year period. We found that effective population size ranged in the hundreds of individuals, which is similar to estimates in other, non-eusocial taxa. Second, we estimated levels of polyandry in V. maculifrons in different years to determine if queen mating system varied over time. We found no significant change in the number or skew of males mated to queens. In addition, mating skew was not significant within V. maculifrons colonies. Therefore, our data suggest that queen mate number may be subject to stabilizing selection in this taxon. Overall, our study provides novel insight into the selective processes operating in eusocial species by analyzing temporal genetic changes within populations.

Introduction of Varroa destructor has not altered honey bee queen mating success in the Hawaiian archipelago

Beekeepers struggle to minimize the mortality of their colonies as a consequence of the parasitic mite Varroa destructor in order to maintain a sustainable managed pollinator population. However, little is known about how varroa mites might diminish local populations of honey bee males (drones) that might affect the mating success of queens. As one of the world’s last localities invaded by varroa mites, the Hawaiian Islands offer a unique opportunity to examine this question by comparing queens mated on mite-infested and mite-free islands. We raised queen bees on four Hawaiian Islands (Kaua‘i, O‘ahu, Maui, and Hawai‘i) and subsequently collected their offspring to determine queen mating frequency and insemination success. No significant difference for mating success was found between the islands with and without varroa mites, and relatively high levels of polyandry was detected overall. We also found a significant association between the number of sperm stored in the queens’ spermathecae and the number of managed colonies within the localities of the queens mated. Our findings suggest that varroa mites, as they currently occur in Hawai‘i, may not significantly reduce mating success of honey bee queens, which provides insight for both the reproductive biology of honey bees as well as the apiculture industry in Hawai‘i.

Phenotypic diversity in red wood ants (Hymenoptera: Formicidae): Is kinship involved?

Phenotypic diversity depends on genotype diversity, but the degree of genotype-by-environment interaction is species-specific. Red wood ants (Formica s. str) are keystone species in boreal forests and very variable phenotypically. These variations are used for species identification and proposed as ecological indicators of anthropogenic disturbances. However, their origin is unknown. Here we aimed to provide a preliminary answer to this question and outline the direction for future research. We determined the interrelation between nest mate worker relatedness (kinship) and the diversity of colour morphs, degree of melanisation and size of the red wood ant, Formica rufa. In Finnish populations of this species polyandry, which involves multiple mating by queens is the principal determinant of the relatedness between workers. We hypothesised, that if phenotypic diversity is a result of genetic diversity, then polyandrous colonies should produce more phenotypically diverse workers. A total of 336 individuals belonging to 20 colonies were used for this study. We collected ants from coniferous and broadleaf forests in Finland, fixed them in 96% alcohol, then digitally photographed, genotyped and analysed the phenotypic variation. The average colony nest mate worker relatedness was used as an estimate of the level of polyandry (more than one if r < 0.6). Our results revealed no associations between the diversity of the phenotypic traits measured and worker kinship in F. rufa. As a further step to reveal the degree of genotype-by-environment interaction in determining the colour traits of the red wood ant we suggest more sophisticated genetic studies indicating the heritability of phenotypic traits between patrilinies and testing of environmental factors such as temperature, humidity, UV-radiation, food and pollution.

Highly promiscuous paternity in mainland and island populations of the endangered Northern Quoll

AbstractPolyandry is a commonly utilized strategy in mammalian reproductive systems, where females engage in mating with multiple males to increase either the genetic diversity or quality of their offspring. Some species also exhibit male semelparity, a peculiar life‐history trait where all or most males within a population begin to die following mating. The northern quoll (Dasyurus hallucatus) possesses both of these reproductive adaptations, and females of this species may produce up to eight young in a single litter. Here we aimed to quantify whether there was any difference in female quolls’ choice of male sires between two genetically distinct populations located in the Pilbara region of Western Australia (one mainland‐dwelling and one island‐dwelling population). The total parentage exclusion probability was 0.9999 for excluding a candidate parent from parentage, given the genotype of a known mother. Overall, we found that every litter had young resulting from multiple males. In some litters, a different male fathered every offspring. Thus, northern quolls demonstrated a greater level of polyandry than has previously been detected in marsupials. Furthermore, females from the less genetically diverse island population exercised mate choice and preferentially bred with males that were, on average, 20% smaller than a different male randomly sampled from the island. There was no detectable difference with regard to male sire body size in the mainland population, indicating a difference of selective pressures for the two populations.

Do metrics of sexual selection conform to Bateman's principles in a wind-pollinated plant?

Bateman's principles posit that male fitness varies more, and relies more on mate acquisition, than female fitness. While Bateman's principles should apply to any organism producing gametes of variable sizes, their application to plants is potentially complicated by the high levels of polyandry suspected for plants, and by variation in the spatial distribution of prospective mates. Here we quantify the intensity of sexual selection by classical Bateman metrics using two common gardens of the wind-pollinated dioecious plant Mercurialis annua. Consistent with Bateman's principles, males displayed significantly positive Bateman gradients (a regression of fitness on mate number), whereas the reproductive success of females was independent of their ability to access mates. A large part of male fitness was explained by their mate number, which in turn was associated with males' abilities to disperse pollen. Our results suggest that sexual selection can act in plant species in much the same way as in many animals, increasing the number of mates through traits that promote pollen dispersal.

Different levels of polyandry in two populations of the funnel-web wolf spider Aglaoctenus lagotis from South America

Populations of a species may show variation in mating systems, especially when the species is widely distributed. Aglaoctenus lagotis is a funnel-web wolf spider distributed in South America and with a ‘central Argentina form’ (CA) and a ‘southern Uruguay form’ (SU). Both forms differ in sexual behaviour, population density and copulatory season. This study evaluates the potential level of polyandry of both forms, sequentially exposing females to different males of their form under laboratory conditions. The number of copulations each female accepted and the characteristics of these sexual encounters were registered. CA females accepted more re-copulations than SU females and seemed to maintain more sexual attractiveness after the first copulation. In neither form was female re-copulation influenced by body characteristics, duration of the first copulation, ejaculation frequency or copulatory body shaking of females. Additionally, the PCA showed that both forms could be separated by their copulation behaviours. The higher level of polyandry in the CA form compared to the SU form suggested in our results adds another difference between these forms, currently under study to determine whether they are different species. This study is the first on mating systems in funnel-web wolf spiders, adding knowledge to the discussion about the evolution of sexual strategies in this group.

Bodyweight-Related Polyandry in the Tobacco Cutworm Moth Spodoptera litura (Lepidoptera: Noctuidae)

Recent studies on polyandry evolution have revolutionized our understanding of sexual selection. Therefore, study on traits in females, such as sensory perception and remating strategies, is expected to disclose a greater role of sexual selection in female evolution. Here, we tested how bodyweights of both sexes affected female and male remating behavior in Spodoptera litura (Fabricius, 1775) (Lepidoptera: Noctuidae). Results show most (74.4%; unmated virgin females may be sexually immature) females and males mated the first time in the second scotophase after eclosion. In the subsequent scotophase, 41.9% once-mated females and 94.1% once-mated males mated the second time with a novel virgin mate. Analyses indicate that female remating probability significantly increased with the increase of her own and the second male’s bodyweight but decreased with the increase of the first male’s bodyweight, while bodyweights of both sexes have no significant effect on male remating probability. Considering the nature of the low level of polyandry (two times on average) and last male precedence in S. litura, we propose that 1) females are more choosy when remating, from which females will benefit indirectly by sequential mate comparison and remate to replace sperm from the previous mates with those from higher quality mates, and 2) males will generally like to remate with any possible females, from which males will gain direct benefit by siring more offspring. The outcome of polyandry rate is likely to be the result of male investment × female choice interactions.

No selection for change in polyandry under experimental evolution.

What drives mating system variation is a major question in evolutionary biology. Female multiple mating (polyandry) has diverse evolutionary consequences, and there are many potential benefits and costs of polyandry. However, our understanding of its evolution is biased towards studies enforcing monandry in polyandrous species. What drives and maintains variation in polyandry between individuals, genotypes, populations and species remains poorly understood. Genetic variation in polyandry may be actively maintained by selection, or arise by chance if polyandry is selectively neutral. In Drosophila pseudoobscura, there is genetic variation in polyandry between and within populations. We used isofemale lines to found replicate populations with high or low initial levels of polyandry and tracked polyandry under experimental evolution over seven generations. Polyandry remained relatively stable, reflecting the starting frequencies of the experimental populations. There were no clear fitness differences between high versus low polyandry genotypes, and there was no signature of balancing selection. We confirmed these patterns in direct comparisons between evolved and ancestral females and found no consequences of polyandry for female fecundity. The absence of differential selection even when initiating populations with major differences in polyandry casts some doubt on the importance of polyandry for female fitness.

Genetic evidence for alloparental care and frequent multiple paternity in the brooding sea star (Leptasterias sp.)

Echinoderms form an abundant and ecologically important group of marine animals, and they are found in nearly every marine environment, from shallow tropical waters to deep polar benthos and even in the pelagic zone. They exhibit a wide diversity of reproductive strategies that range from broadcasting millions of gametes, with no parental care, to internal brooding of a few embryos for several weeks. While many echinoderm species have become model systems for studies of community ecology, evolutionary genetics, and development biology, very little is known about the distribution of mating and reproductive success in natural populations. In this study, we examined patterns of genetic maternity and paternity in the six-rayed sea star Leptasterias sp., an important predator of many intertidal communities and a species that exhibits maternal care of embryos. We used next-generation sequencing to rapidly develop informative microsatellite markers for this species, and used these markers to genotype 439 juveniles across 15 broods collected from the intertidal in Fogarty Creek, Oregon, USA. Our data show an unambiguous pattern of multiple paternity in all but one clutch examined, with some broods showing some of the highest levels of polyandry reported for a marine invertebrate. Moreover, we detected two cases of mixed maternity in which a female sea star carried another mother’s offspring mixed with her own. Alloparental care by females is rare, and since female Leptasterias do not eat during the 40–60 days brooding period, this expensive behavior may provide a useful system for examining the evolutionary costs and benefits of parental care in dynamic intertidal environments.

Sex peptide receptor-regulated polyandry modulates the balance of pre- and post-copulatory sexual selection in Drosophila

Polyandry prolongs sexual selection on males by forcing ejaculates to compete for fertilisation. Recent theory predicts that increasing polyandry may weaken pre-copulatory sexual selection on males and increase the relative importance of post-copulatory sexual selection, but experimental tests of this prediction are lacking. Here, we manipulate the polyandry levels in groups of Drosophila melanogaster by deletion of the female sex peptide receptor. We show that groups in which the sex-peptide-receptor is absent in females (SPR-) have higher polyandry, and – as a result – weaker pre-copulatory sexual selection on male mating success, compared to controls. Post-copulatory selection on male paternity share is relatively more important in SPR- groups, where males gain additional paternity by mating repeatedly with the same females. These results provide experimental evidence that elevated polyandry weakens pre-copulatory sexual selection on males, shifts selection to post-copulatory events, and that the sex peptide pathway can play a key role in modulating this process in Drosophila.

High levels of polyandry, but limited evidence for multiple paternity, in wild populations of the western rock lobster (Panulirus cygnus).

Polyandry, where multiple mating by females results in the temporal and spatial overlap of ejaculates from two or more males, is taxonomically widespread and occurs in varying frequencies within and among species. In decapods (crabs, lobsters, crayfish, and prawns), rates of polyandry are likely to be variable, but the extent to which patterns of multiple paternity reflect multiple mating, and thus are shaped by postmating processes that bias fertilization toward one or a subset of mated males, is unclear. Here, we use microsatellite markers to examine the frequency of multiple mating (the presence of spermatophores from two or more males) and patterns of paternity in wild populations of western rock lobster (Panulirus cygnus). Our data confirm that >45% of females had attached spermatophores arising from at least two males (i.e., confirming polyandry), but we found very limited evidence for multiple paternity; among 24 clutches sampled in this study, only two arose from fertilizations by two or more males. Single inferred paternal genotypes accounted for all remaining progeny genotypes in each clutch, including several instances when the mother had been shown to mate with two or more males. These findings highlight the need for further work to understand whether polyandry is adaptive and to uncover the mechanisms underlying postmating paternity biases in this system.

Low level of polyandry constrains phenotypic plasticity of male body size in mites.

Polyandry, i.e. females mating with multiple males, is more common than previously anticipated and potentially provides both direct and indirect fitness benefits to females. The level of polyandry (defined by the lifetime number of male mates of a female) is an important determinant of the occurrence and intensity of sexual selection acting on male phenotypes. While the forces of sexual selection acting on phenotypic male traits such as body size are relatively well understood, sexual selection acting on phenotypic plasticity of these traits is unexplored. We tackled this issue by scrutinizing the link between polyandry and phenotypic plasticity of male body size in two sympatric plant-inhabiting predatory mite species, Phytoseiulus persimilis and Neoseiulus californicus. These two species are similar in life history, ecological niche requirements, mating behavior, polygyny and female body size plasticity but strikingly differ in the level of both polyandry and phenotypic plasticity of male body size (both lower in P. persimilis). We hypothesized that deviations from standard body size, i.e. the size achieved under favorable conditions, incur higher costs for males in the less polyandrous P. persimilis. To test our hypotheses, we conducted two experiments on (i) the effects of male body size on spermatophore transfer in singly mating females and (ii) the effects of mate sequence (switching the order of standard-sized and small males) on mating behavior and paternity success in doubly mating females. In P. persimilis but not N. californicus, small males transferred fewer but larger spermatophores to the females; in both species, females re-mated more likely with standard-sized following small than small following standard-sized males; in P. persimilis, first standard-sized males sired a higher proportion of offspring produced after re-mating by the female than first small males, whereas in N. californicus the paternity success of small and standard-sized males was independent of the mating sequence. Based on our results and pertinent previous studies, which showed that females of P. persimilis, but not N. californicus, prefer mating with standard-sized over small males and allow them fertilizing more eggs, the lack of interspecific difference in female body size plasticity, and the absence of any clue pointing at a role of natural selection, we suggest that the interspecific difference in male body size plasticity is sexually selected. Our study provides an indication of sexual selection constraining plasticity of male phenotypes, suggesting that the level of polyandry may be an important co-determinant of the level of phenotypic plasticity of male body size.

Polyandry across Behavioral Classes in Female Spruce Budworm

Reproduction in spruce budworm, Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae), is characterized by sedentary oviposition in the natal forest patch early in life (gravid females are incapable of flight due to their heavy abdomen) followed by windborne migrations among females that have laid >50% of their eggs; the nature of migrations (facultative or obligatory) remains unknown. The incidence of polyandry (females with more than one spermatophore in their reproductive tract) was evaluated for several thousand field-collected female budworms (data professionally archived at Canadian Forest Service) using an array of sampling procedures that can be delineated along four behavioral classes: (1) resident females collected on host trees; (2) in-flight females captured while foraging in forest canopies; (3) migrant females captured above tree canopies; and (4) females collected postmortem on drop trays. Overall, polyandry increased over time (reflecting the ageing of local populations) and with female body size (likely due to male mating preference for large, most fecund females). Polyandry did not increase postmortem realized fecundity of females. The level of polyandry was lowest among migrants, intermediate for in-flight and resident females, and highest for naturally dead females. Sedentary reproduction among young female budworms may limit gene flow and increase the risk of inbreeding; a low level of polyandry among migrants may thus be due to females not only seeking novel habitats for their progeny but also mating partners that are not closely related genetically.

Polyandry, genetic diversity and fecundity of emigrating beetles: understanding new foci of infestation and selection

The frequency of polyandry and its ecological (and therefore selective) advantages remain unclear, especially in the field, where such tests are seldom conducted. We quantified the fecundity and level of polyandry in field populations of two stored grain beetles, Tribolium castaneum (Herbst) and Rhyzopertha dominica (F.), by comparing resident with dispersing individuals at common sites. Almost all females caught in flight had mated, with paternity analysis from 110 parent–offspring arrays revealing that most females had mated with more than one male (T. castaneum: 90.6, R. dominica: 70.2%). No difference in the extent of polyandry between beetles collected from grain in storage and beetles caught in flight was detected for either species, and the degree of polyandry did not impact overall fecundity. Levels of polyandry were similar to those in recently established (first generation) laboratory cultures of both species. Our results provide the first direct evidence of polyandry in wild populations of T. castaneum and R. dominica, and that females that have mated several times have the potential to produce offspring of multiple genotypes in the field. Females thus invade resource patches (whether previously colonised or not) with considerable genetic diversity to distribute across their offspring, an advantage in a newly colonised site because it increases the chances of her offspring establishing there. This advantageous consequence of polyandry to dispersing individuals, and the fact that most of the individual beetles sampled in the field had mated multiple times, provides justification as to why polyandry should not be viewed as an evolutionary paradox.