Evolution Of Polyandry Research Articles

Low queen mating frequency in the seed-harvester ant Pogonomyrmex (Ephebomyrmex) pima: implications for the evolution of polyandry

The evolution of polyandry is a central problem in the study of insect mating systems, and both material and genetic benefits have been proposed to offset the presumed costs of multiple mating. Although most eusocial Hymenoptera queens mate with just one or occasionally two males, high levels of polyandry are exhibited by several taxa, including seed-harvester ants of the genus Pogonomyrmex. Previous studies of queen mating frequency in Pogonomyrmex have focused on monogynous (one queen per colony) species in the subgenus Pogonomyrmex. We performed a genetic mother–offspring analysis of mating frequency in Pogonomyrmex (Ephebomyrmex) pima, a queen-dimorphic species with dealate and intermorph queens that differ in colony structure (intermorph colonies contain multiple queens). Our results demonstrate that both dealate and intermorph queens of P. (E.) pima are typically single maters, unlike their congeners analyzed thus far. Polyandry appears to be a derived trait in Pogonomyrmex, but comparative tests between P. (E.) pima queen morphs and across the genus provide no evidence that it evolved as an adaptation to increase genetic diversity within colonies or to obtain more sperm, respectively.

Genetic diversity promotes homeostasis in insect colonies

Although most insect colonies are headed by a singly mated queen, some ant, wasp and bee taxa have evolved high levels of multiple mating or 'polyandry'. We argue here that a contributing factor towards the evolution of polyandry is that the resulting genetic diversity within colonies provides them with a system of genetically based task specialization, enabling them to respond resiliently to environmental perturbation. An alternate view is that genetic contributions to task specialization are a side effect of multiple mating, which evolved through other causes, and that genetically based task specialization now makes little or no contribution to colony fitness.

Good genes, genetic compatibility and the evolution of polyandry: use of the diallel cross to address competing hypotheses

Genetic benefits can enhance the fitness of polyandrous females through the high intrinsic genetic quality of females' mates or through the interaction between female and male genes. I used a full diallel cross, a quantitative genetics design that involves all possible crosses among a set of genetically homogeneous lines, to determine the mechanism through which polyandrous female decorated crickets (Gryllodes sigillatus) obtain genetic benefits. I measured several traits related to fitness and partitioned the phenotypic variance into components representing the contribution of additive genetic variance ('good genes'), nonadditive genetic variance (genetic compatibility), as well as maternal and paternal effects. The results reveal a significant variance attributable to both nonadditive and additive sources in the measured traits, and their influence depended on which trait was considered. The lack of congruence in sources of phenotypic variance among these fitness-related traits suggests that the evolution and maintenance of polyandry are unlikely to have resulted from one selective influence, but rather are the result of the collective effects of a number of factors.

The quantitative genetic basis of polyandry in the parasitoid wasp, Nasonia vitripennis

Understanding the evolution of female multiple mating (polyandry) is crucial for understanding sexual selection and sexual conflict. Despite this interest, little is known about its genetic basis or whether genetics influences the evolutionary origin or maintenance of polyandry. Here, we explore the quantitative genetic basis of polyandry in the parasitoid wasp Nasonia vitripennis, a species in which female re-mating has been observed to evolve in the laboratory. We performed a quantitative genetic experiment on a recently collected population of wasps. We found low heritabilities of female polyandry (re-mating frequency after 18 h), low heritability of courtship duration and a slightly higher heritability of copulation duration. However, the coefficients of additive genetic variance for these traits were all reasonably large (CV(A)>7.0). We also found considerable dam effects for all traits after controlling for common environment, suggesting either dominance or maternal effects. Our work adds to the evidence that nonadditive genetic effects may influence the evolution of mating behaviour in Nasonia vitripennis, and the evolution of polyandry more generally.

Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina

Understanding why females mate multiply is a major issue in evolutionary ecology. We investigated the consequences of an asynchronous arrival pattern on male competition and multiple paternity in the apparently monoandrous agile frog (Rana dalmatina). The largest frogs arrived first and both males and females lost weight significantly during the spawning period. Asynchronous arrival at breeding sites resulted in a male-biased operational sex ratio (OSR). The OSR was more strongly male-biased at the beginning and at the end of the breeding period when the number of satellite males increased. All females mated only once, but multiple paternity within clutches occurred at the beginning and the end of the breeding period. The influence of asynchronous arrival and biased sex ratio suggests that reduced variance or bet-hedging promoting female fitness had only a reduced role in the evolution of polyandry, and polyandry is likely to be associated with male benefits. Polyandry in frogs can be explained either by forced mating as a result of sexual conflict or by clutch piracy. By modifying intrasexual competition, asynchronous arrival and changes in OSR may have a decisive influence upon the evolution of mating systems and favour both polyandry and stable coexistence of alternative mating behaviour.

FAITHFUL WITHOUT CARE: THE EVOLUTION OF MONOGYNY

The traditional paradigm of male polygamy and female monogamy has been replaced by the recognition that both sexes may typically mate with several partners. As a consequence, much attention has focused on the evolution of polyandry, while the evolutionary significance of monogyny (male monogamy) remains poorly understood. Monogyny, a taxonomically widespread mating system that includes dramatic examples of male self-sacrifice, is predicted when the benefits of paternal investment exceed those of searching for additional mates. However, monogyny also occurs in animals lacking paternal investment, instead representing a form of paternity protection. It has been suggested that such mating systems are expected where the costs of mate search for males are high. However, this argument fails to recognize that if there is a low probability of a male finding a mate, then there may be a high probability that he will not need to defend his paternity. Using a mathematical model, we show that monogyny as a means of increasing paternity is favored when the sex ratio is male biased, but not necessarily by high search costs. The importance of a male-biased sex ratio for the evolution of monogyny is supported by various empirical studies.

FAITHFUL WITHOUT CARE: THE EVOLUTION OF MONOGYNY

The traditional paradigm of male polygamy and female monogamy has been replaced by the recognition that both sexes may typically mate with several partners. As a consequence, much attention has focused on the evolution of polyandry, while the evolutionary significance of monogyny (male monogamy) remains poorly understood. Monogyny, a taxonomically widespread mating system that includes dramatic examples of male self-sacrifice, is predicted when the benefits of paternal investment exceed those of searching for additional mates. However, monogyny also occurs in animals lacking paternal investment, instead representing a form of paternity protection. It has been suggested that such mating systems are expected where the costs of mate search for males are high. However, this argument fails to recognize that if there is a low probability of a male finding a mate, then there may be a high probability that he will not need to defend his paternity. Using a mathematical model, we show that monogyny as a means of increasing paternity is favored when the sex ratio is male biased, but not necessarily by high search costs. The importance of a male-biased sex ratio for the evolution of monogyny is supported by various empirical studies.

Male accessory gland size and the evolutionary transition from single to multiple mating in the fungus-gardening ants

Polyandry in hymenopteran social insects is surprisingly rare, despite its likely colony-level fitness benefits. Ordinarily, a male's fitness will be at odds with that of a colony when the genetic representation within it is diluted by multiple mating by the queen. Consequently, males are expected to be under selection to limit female re-mating, for example via secretions of their accessory glands. I hypothesized that if accessory glands in some way regulate female mating frequency, an evolutionary transition from single to multiple mating would likely be accompanied with a change in the morphology of the accessory glands. The accessory gland morphology was examined in the fungus-gardening ants, which have made a single transition from single to multiple mating. The evolution of polyandry within this clade corresponds to the loss of male accessory glands, lending tentative support to the idea that they may be involved in regulating mating frequency.MAG Male accessory gland

Male reproductive investment and queen mating-frequency in fungus-growing ants

Sperm number and male accessory gland compounds are often important determinants of male mating success but have been little studied in social insects. This is because mating in social insects is often difficult to manipulate experimentally, and first evidence for an explicit influence of accessory gland secretions on male mating success in social insects was obtained only recently. Here we perform a comparative analysis of male sexual organs across 11 species of attine fungus-growing ants, representing both genera with single- and multiple-queen mating. We found that the general morphology of the male sexual organs was very similar across all species, but the relative sizes of the accessory glands and the sperm-containing accessory testes vary significantly across species. Small testes and large accessory glands characterize species with singly mated queens, whereas the opposite is found in species with multiply mated queens. However, in the social parasite Acromyrmex insinuator, in which queens have secondarily reverted to single mating, males have accessory gland characteristics reminiscent of the lower attine ants, but without having significantly reduced their investment in sperm production. We hypothesize that the main function of accessory gland compounds in attine ants is to monopolize male paternity in similar ways as known from other social insects. This would imply that the evolution of polyandry in the terminal clade of the fungus-growing ants (the leafcutter ants) has resulted in selection for decreased investment by males in accessory gland secretions and increased investment in sperm number, in response to sperm competition for sperm storage.

Male accessory gland size and the evolutionary transition from single to multiple mating in the fungus-gardening ants.

Polyandry in hymenopteran social insects is surprisingly rare, despite its likely colony-level fitness benefits. Ordinarily, a male's fitness will be at odds with that of a colony when the genetic representation within it is diluted by multiple mating by the queen. Consequently, males are expected to be under selection to limit female re-mating, for example via secretions of their accessory glands. I hypothesized that if accessory glands in some way regulate female mating frequency, an evolutionary transition from single to multiple mating would likely be accompanied with a change in the morphology of the accessory glands. The accessory gland morphology was examined in the fungus-gardening ants, which have made a single transition from single to multiple mating. The evolution of polyandry within this clade corresponds to the loss of male accessory glands, lending tentative support to the idea that they may be involved in regulating mating frequency.

THE EVOLUTION OF FEMALE MULTIPLE MATING IN SOCIAL HYMENOPTERA

The evolution of female multiple mating is a highly controversial topic, especially in social insects. Here we analyze, using comparative analyses and simulation models, the merits of two major contending hypotheses for the adaptive value of polyandry in this group. The hypotheses maintain that, respectively, the resulting genotypic diversity among offspring within a colony: (1) mitigates against the effects of parasites; or (2) favors adaptive division of labor. Only two of 11 phylogenetically uncontrolled comparative analyses supported an association between polyandry and the complexity of division of labor (measured here using worker caste polymorphism or polyethism) as proposed by hypothesis 2, and after controlling for phylogeny there were no significant associations. In contrast, a previous study demonstrated such an association for parasite load as expected under hypothesis 1. In addition, we used simulation models to track the spread of an initially rare allele for double mating in a population of single-mating alleles, thus analyzing the crucial first step from monandry to polyandry. We find that double mating evolves consistently under antagonistic coevolution given that parasites exert sufficient selection intensity. In contrast, selection for enhanced division of labor resulted in only an erratic appearance of polyandry in highly (and mostly negatively) autocorrelated environments where no coevolutionary dynamics were allowed. Together, we interpret these results to suggest that parasites, and the antagonistic coevolutionary pressures they exert, may play an important role in the evolution of polyandry in social hymenopteran populations.

Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits.

Sperm competition is widely recognized as a potent force in evolution, influencing male behavior, morphology, and physiology. Recent game theory analyses have examined how sperm competition can influence the evolution of ejaculate expenditure by males and the morphology of sperm contained within ejaculates. Theoretical analyses rest on the assumption that there is sufficient genetic variance in traits important in sperm competition to allow evolving populations to move to the evolutionarily stable equilibrium. Moreover, patterns of genotypic variation can provide valuable insight into the nature of selection currently acting on traits. However, our knowledge of genetic variance underlying traits important in sperm competition is limited. Here we examine patterns of phenotypic and genotypic variation in four sperm competition traits in the dung beetle Onthophagus taurus. Testis weight, ejaculate volume, and copula duration were found to have high coefficients of additive genetic variation (CV(A)S), which is characteristic of fitness traits and traits subject to sexual selection. Heritabilities were high, and there was some evidence for Y-linked inheritance in testis weight. In contrast, sperm length had a low CV(A), which is characteristic of traits subject to stabilizing selection. Nevertheless, there was little residual variance so that the heritability of sperm length exceeded 1.0. Such a pattern is consistent with Y-linked inheritance in sperm length. Interestingly, we found that testis weight and sperm length were genetically correlated with heritable male condition. This finding holds important implications for potential indirect benefits associated with the evolution of polyandry.

Biased sperm use by polyandrous queens of the ant Proformica longiseta

The occurrence and genetic effects of polyandry were studied in the ant Proformica longiseta using three microsatellite markers. The average queen mating frequency (QMF) estimated from the sperm dissected from the spermathecae of 61 queens was 2.4 with 69% of the queens being multiply mated. QMF estimated from worker offspring in a subsample of eight monogynous colonies was 3.5, but the effective paternity (m e,p) was only 1.23. The difference between these values reflected unequal sperm use by the queens. Most colonies of P. longiseta were polygynous and the average relatedness among workers was 0.35. Polyandry thus added only marginally to the genetic diversity of colonies, and our results gave little support to the genetic-variability hypothesis for explaining polyandry. Diploid male load was low, as only 1% of males were diploid. A large majority (92%) of nests produced one sex only, with males produced in colonies that had higher than average worker relatedness. This contradicted the predictions derived from worker control of sex ratios. Males produced enough sperm to fill the spermathecae of several queens. Thus, the results indicated that diploid male load, sperm limitation and sex ratio conflict are also unlikely explanations of polyandry. Plausible hypotheses for polyandry include mating by convenience, as the sex ratio is male biased and the mating costs to a female can be low because the females are wingless and have no mating flight. The observed unequal sperm use furthermore points to sperm choice and sperm competition as important factors in the evolution of polyandry.

EVOLUTION OF EJACULATES: PATTERNS OF PHENOTYPIC AND GENOTYPIC VARIATION AND CONDITION DEPENDENCE IN SPERM COMPETITION TRAITS

Sperm competition is widely recognized as a potent force in evolution, influencing male behavior, morphology, and physiology. Recent game theory analyses have examined how sperm competition can influence the evolution of ejaculate expenditure by males and the morphology of sperm contained within ejaculates. Theoretical analyses rest on the assumption that there is sufficient genetic variance in traits important in sperm competition to allow evolving populations to move to the evolutionarily stable equilibrium. Moreover, patterns of genotypic variation can provide valuable insight into the nature of selection currently acting on traits. However, our knowledge of genetic variance underlying traits important in sperm competition is limited. Here we examine patterns of phenotypic and genotypic variation in four sperm competition traits in the dung beetle Onthophagus taurus. Testis weight, ejaculate volume, and copula duration were found to have high coefficients of additive genetic variation (CVAs), which is characteristic of fitness traits and traits subject to sexual selection. Heritabilities were high, and there was some evidence for Y-linked inheritance in testis weight. In contrast, sperm length had a low CVA, which is characteristic of traits subject to stabilizing selection. Nevertheless, there was little residual variance so that the heritability of sperm length exceeded 1.0. Such a pattern is consistent with Y-linked inheritance in sperm length. Interestingly, we found that testis weight and sperm length were genetically correlated with heritable male condition. This finding holds important implications for potential indirect benefits associated with the evolution of polyandry.

The evolution of polyandry: an examination of the genetic incompatibility and good-sperm hypotheses

Abstract I have examined the adaptive significance of polyandry using the Australian field cricket Teleogryllus oceanicus. Previous studies of polyandry have examined differences in offspring production by females mated multiply to a single male or females mated multiply to different males. Here I combine this approach with a study of parentage of offspring produced in the later group. Females mated to two different males had a higher proportion of their eggs hatching than did females mating twice with a single male. Offspring fitness parameters were not effected. There was little evidence to suggest that females elevate their hatching success via fertilizing their eggs with sperm from genetically compatible males. Although the average paternity points towards random sperm mixing, there was considerable individual variation in sperm competition success. Patterns of parentage were consistent across females mating twice or four times. Sperm competition success was not related to offspring viability or performance. Thus, the notion that competitively superior sperm produce competitively superior offspring is not supported either. The mechanism underlying increased hatching success with polyandry requires further study.

Mating frequency, colony size, polyethism and sex ratio in fungus-growing ants (Attini)

The mating frequency of queens was estimated for eight attine ant species, Myrmicocrypta ednaella, Apterostigma mayri, Cyphomyrmex costatus, C. rimosus (four lower attines), Trachymyrmex isthmicus, Serico-myrmex amabalis, Acromyrmex octospinosus and Atta colombica (four higher attines), and correlated to colony size, worker polyethism, and sex ratio. Mating frequency was calculated from within-colony relatedness estimated by CAP-PCR DNA fingerprinting. Most queens of lower attines and T. isthmicus mated with only one male, while those of the three higher attines mated with multiple males. Mating frequency was positively correlated with colony size. Polyethism among workers was dependent on worker age in lower attines but on body size in higher attines, suggesting some correlation between mating frequency (i.e., within-colony gene diversity) and caste complexity. The sex ratio was biased toward females in species where the mating frequency equaled one, but toward males in species where the mating frequency was greater than two. Changing in nest site from ground surface to deep underground may have facilitated the evolution of large colony size in Attini, and this may have resulted in the evolution of polyandry (a queen mates with multiple males). With the evolution of polyandry in higher attines, Atta and Acromyrmex in particular have generated high genetic diversity within their colonies and complex social structures.

Facultative Sex Allocation by Workers and the Evolution of Polyandry by Queens in Social Hymenoptera

Recent theoretical and empirical studies have shown that worker Hymenoptera may facultatively bias colony sex allocation according to the mating frequency of their queen, which results in more male-biased allocation in colonies with queens mated to an above-average number of males. Given the occurrence of this worker reproductive strategy, and because the queen-optimum sex-allocation ratio is more male biased than the population-wide worker-optimum ratio, individual queens may be able to enhance their inclusive fitness by mating with additional males. Using inclusive fitness models, we examine the fitness of single-, double-, and treble-mated queens in a population in which workers facultatively bias colony sex allocation with respect to queen mating frequency. We show that the relative inclusive fitness of double-versus single-mated queens can vary from 3:1 to 1:1. Low error rates in the assessment of queen mating frequency by workers, low worker production of males, low proportions of double-mated queens, and other factors enhance the relative fitness of the double-mated queens. Inclusive fitness gains to double-mated queens through more male-biased colony sex allocation must compensate for any costs arising from making additional matings. Double mating can be favored under some conditions but disfavored under others. Double- and single-mated queens may have equal total fitness at an intermediate proportion of double-mated queens in the population, which leads to a mixed mating strategy. We develop three nonexclusive scenarios under which treble mating can potentially be favored over double mating. The conditions favoring treble mating are more restrictive than those favoring double mating.

Diploid males and colony-level selection inFormicaants

It is suggested that the evolution of polyandry by social hymenopteran queens is caused by colony-level selection, either because polyandry affects the distribution of non-functional diploid males in colonies (the load hypothesis) or because it increases the genetic diversity of the worker force (the diversity hypothesis). Diploid males that arise from fertilized eggs thai are homozygous at the sex-determining locus (or loci) are inviable or infertile. Models of the load hypothesis analysed in this study suggest that slow growth and high mortality of colonies with diploid males favour single mating by queens. The longer the period ol colony growth (the period with selective differences) and the heavier the mortality, the stronger is the selection for monandry. The load hypothesis also predicts an association between monogyny and monandry. In contrast, the diversity hypothesis predicts an association between monogyny and polyandry, as multiple mating offers a way by which a monogynous colony could increase...

Peahens lay more eggs for peacocks with larger trains

Reproduction is costly and individual decisions about when and how much to invest in reproduction will relate to potential benefits in terms of offspring survivorship or mating success. For those organisms that can reproduce more than once, individuals should invest relatively more in reproduction when the potential benefits are high. If females gain directly or indirectly from choosing attractive, highly ornamented males, then it could be predicted that females mated to these males should invest more in reproduction. Here we report the first test of this prediction for a lekking species, peafowl (Pavo cristatus), in which males do not provide resources for offspring, and females prefer to mate with those males that possess the most elaborate trains. We find that peahens randomly mated to males that vary in the degree of ornament produce more eggs for those peacocks with more elaborate trains. We could find no evidence to support the possibility that this difference arises as a result of difference between males in their ability to fertilize eggs.

The evolution of polyandry by queens in social Hymenoptera: the significance of the timing of removal of diploid males

Multiple mating by queens in social Hymenoptera with single locus sex determination may be an adaptation to reduce the effect of genetic load caused by the production of diploid males, if there is a concave relationship between queen fitness and the proportion of diploid male offspring in the colony. In this situation queens should be selected to reduce the variance in the production of diploid male offspring by multiple mating. It has been suggested that this concave relationship occurs in species such as the honey bee, Apis mellifera, in which reproduction occurs near the peak of colony population. This paper suggests that the timing of diploid male removal may influence mating frequency, with early removal of diploid males favoring multiple mating and late removal of diploid males favoring single mating. This idea is explored in two ways. A mathematical model shows that cell use in the brood area of species that rear young in cells will be more efficient with multiple mating. This would favor multiple mating in species, such as the honey bee, in which brood rearing is constrained by the usable area of the brood chamber. Secondly, comparison of polyandrous honey bees (early removal of diploid males as young larvae) with monandrous fire ants, Solenopsis invicta, and Melipona bees (non-removal of immature diploid males) suggests that in the species without diploid male removal, variance reduction may reduce queen fitness. Suggestions are made for testing this hypothesis.