A test of neuroecological predictions using paperwasp caste differences in brain structure (Hymenoptera: Vespidae)

Adaptive brain architecture hypotheses predict brain region investment matches the cognitive and sensory demands an individual confronts. Social hymenopteran queen and worker castes differ categorically in behavior and physiology leading to divergent sensory experiences. Queens in mature colonies are largely nest-bound while workers depart nests to forage. We predicted social paperwasp castes would differ in tissue allocation among brain regions. We expected workers to invest relatively more than queens in neural tissues that process visual input. As predicted, we found workers invested more in visual relative to antennal processing than queens both in peripheral sensory lobes and in central processing brain regions (mushroom bodies). Although we did not measure individual brain development changes, our comparative data provide a preliminary test of mechanisms of caste differences. Paperwasp species differ in the degree of caste differentiation (monomorphic versus polymorphic castes) and in colony structure (independent- versus swarm-founding); these differences could correspond to the magnitude of caste brain divergence. If caste differences resulted from divergent developmental programs (experience-expectant brain growth), we predicted species with morphologically distinct queens, and/or swarm-founders, would show greater caste divergence of brain architecture. Alternatively, if adult experience affected brain plasticity (experience-dependent brain growth), we predicted independent-founding species would show greater caste divergence of brain architecture. Caste polymorphism was not related to the magnitude of queen-worker brain differences, and independent-founder caste brain differences were greater than swarm-founder caste differences. Greater caste separation in independent-founder brain structure suggests a role for adult experience in the development of caste-specific brain anatomy.     

Protein content of spermatophores in relation to monandry/polyandry in butterflies

The evolution of a mating system, and specifically mating frequency, is dependent on the costs and benefits to both sexes of mating once or several times. In butterflies, males transfer a spermatophore that contains both sperm and accessory gland products. Accessory gland substances contain nutrients which, in some species, females use to increase their reproductive output and longevity. Nutrients contained in these packaged ejaculates represent investment by males in reproduction. Consequently, the nutritional composition of spermatophores may vary depending on the mating system. There are two lines of arguments concerning the evolution of the nutrient content of ejaculates. One hypothesis argues that male nuptial gifts evolved in the context of certainty of paternity and ease of finding mates; thus spermatophores of polyandrous males (with lower certainty of paternity and greater ease of finding mates) should contain less protein than those of monandrous males, since more spermatophores are produced on average. The other hypothesis argues that polyandry evolved in the context of maximization of male transfer of nutrients to females, and hence spermatophores of polyandrous males should contain more protein than those of monandrous males. In an attempt to distinguish between these two hypotheses, we determined how protein content of ejaculates varied with the degree of polyandry in nine species of pierid and two species of satyrid butterflies. We found that both relative ejaculate mass and protein content increased with the degree of polyandry. Hence our results are consistent with the view that polyandry has evolved in the context of male transfer of nutrients to females, and provides another example of a male adaptation to multiple mating in butterflies.     

Sex determination and the evolution of polyandry in honey bees (Apis mellifera)

Many hypotheses attempt to explain why queens of social insects mate multiply. We tested the sex locus hypothesis for the evolution of polyandry in honey bees (Apis mellifera). A queen may produce infertile, diploid males that reduce the viability of worker brood and, presumably, adversely affect colony fitness. Polyandry reduces the variance in diploid male production within a colony and may increase queen fitness if there are non-linear costs associated with brood viability, specifically if the relationship between brood viability and colony fitness is concave. We instrumentally inseminated queens with three of their own brothers to vary brood viability from 50% to 100% among colonies. We measured the colonies during three stages of their development: (1) colony initiation and growth, (2) winter survival, and (3) spring reproduction. We found significant relationships between brood viability and most colony measures during the growth phase of colonies, but the data were too variable to distinguish significant non-linear effects. However, there was a significant step function of brood viability on winter survival, such that all colonies above 72% brood viability survived the winter but only 37.5% of the colonies below 72% viability survived. We discuss the significance of this and other "genetic diversity" hypotheses for the evolution of polyandry.     

Behavioral regulation of genetic caste determination in a Pogonomyrmex population with dependent lineages

The fate of a social insect colony is partially determined by its ability to allocate individuals to the caste most appropriate for the requirements for growth, maintenance, and reproduction. In pairs of dependent lineages of Pogonomyrmex barbatus, the allocation of individuals to the queen or worker caste is constrained by genotype, a system known as genetic caste determination (GCD). In mature GCD colonies, interlineage female eggs develop into sterile workers, while intralineage eggs become reproductively capable queens. Although the population-level consequences of this system have been intensively studied, the proximate mechanisms for GCD remain unknown. To elucidate these mechanisms, we brought newly mated queens into the laboratory and allowed them to establish colonies, nearly half of which unexpectedly produced virgin queens only seven months after colony founding. We genotyped eggs, workers, and the virgin queens from these colonies. Our results showed that queens in young colonies produce both interlineage and intralineage eggs, demonstrating that queens of GCD colonies indiscriminately use sperm of at least two lineages to fertilize their eggs. Intralineage eggs were more frequent in colonies producing virgin queens. These findings suggest that intralineage eggs are predetermined to become queens and that workers may cull these eggs when colonies are not producing queens. Virgin queens produced by young GCD colonies were smaller than field-caught virgin queens, and often had developmental problems. Hence, they are probably nonfunctional and represent an intense resource drain for developing colonies, not a contribution to colony fitness.     

Promiscuous honeybee queens generate colonies with a critical minority of waggle-dancing foragers

Honeybees present a paradox that is unusual among the social Hymenoptera: extremely promiscuous queens generate colonies of nonreproducing workers who cooperate to rear reproductives with whom they share limited kinship. Extreme polyandry, which lowers relatedness but creates within-colony genetic diversity, produces substantial fitness benefits for honeybee queens and their colonies because of increased disease resistance and workforce productivity. However, the way that these increases are generated by individuals in genetically diverse colonies remains a mystery. We assayed the foraging and dancing performances of workers in multiple-patriline and single-patriline colonies to discover how within-colony genetic diversity, conferred to colonies by polyandrous queens, gives rise to a more productive foraging effort. We also determined whether the initiation by foragers of waggle-dance signaling in response to an increasing sucrose stimulus (their dance response thresholds) was linked to patriline membership. Per capita, foragers in multiple-patriline colonies visited a food source more often and advertised it with more waggle-dance signals than foragers from single-patriline colonies, although there was variability among multiple-patriline colonies in the strength of this difference. High-participation patrilines emerged within multiple-patriline colonies, but their more numerous foragers and dancers were neither more active per capita nor lower-threshold dancers than their counterparts from low-participation patrilines. Our results demonstrate that extreme polyandry does not enhance recruitment effort through the introduction of low-dance-threshold, high-activity workers into a colony’s population. Rather, genetic diversity is critical for injecting into a colony’s workforce social facilitators who are more likely to become engaged in foraging-related activities, so boosting the production of dance signals and a colony’s responsiveness to profitable food sources.     

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. Received: 26 October 1999 / Revised: 25 May 2000 / Accepted: 24 June 2000     

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.     

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.     

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

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

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.     

Biased sperm use by polyandrous queens of the ant<Emphasis Type="Italic"> Proformica longiseta</Emphasis>

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.     

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     

Colony genetic diversity affects task performance in the red ant Myrmica rubra

High relatedness and low genetic diversity among individuals in a group is generally considered crucial to the evolution of cooperative behaviour. However, in about a third of social insect species, intracolonial genetic diversity is increased because of derived polyandry (multiple mating by queens) and/or polygyny (multiple reproductive queens). Several studies have shown that increased intracolonial genetic diversity can enhance task performance in honey bees, but evidence of such effect in other social insects is still lacking. Why increased genetic diversity has evolved in some, but not all species, is a fundamental question in sociobiology. In this study, we investigated the effect of intracolonial genetic diversity on the task of nest migration, using the facultatively polyandrous and polygynous red ant Myrmica rubra. Genetic diversity significantly affected migration speed, but its effects were context dependent. Migration speed correlated positively with genetic diversity in one experiment in which migrations were into a known nest site, due to quicker transfer of brood into the new nest once consensus was reached. However, in a another experiment in which migration included scouting for new nest sites, migration speed correlated negatively with genetic diversity, due to slower discovery of new nest sites and slower transfer of brood into the new nest. Our results show for the first time that genetic diversity affects task performance in a social insect other than the honeybee, but that it can produce contrasting effects under different conditions.     

Heirs and spares: caste conflict and excess queen production in Melipona bees

The caste conflict hypothesis states that there is potential conflict over the caste fate of totipotent immature females in social insects. In most species, an immature female has little control over her fate because workers control her nutrition. However, in Melipona bees, immature females should have considerable control over their own caste fate because they develop on a provision mass in a sealed cell, and because queens are not larger than workers. This may explain why, in Melipona, large numbers of queens are reared only to be executed. (Because Melipona colonies are founded by swarms very few reproductive opportunities for adult queens occur.) This study uses a one-locus genetic model to determine the optimum proportion of females that should develop into queens from the perspective of immature totipotent females who control their own caste fate. For a population in which all colonies are headed by a single, single-mated queen, which is the typical situation in Melipona, the optimum rises from 14-20% as male production by workers declines from 100% to zero. This agrees well with previous studies which, collectively, give an average of 22% of females developing into queens.     

Caste allocation in litter Pheidole: lessons from plant defense theory

The allocation to growth, defense and reproduction varies in social insects within a species' life cycle and between species. A life cycle model (Oster and Wilson 1978) generally failed to predict caste allocation in small litter-nesting colonies of Neotropical Pheidole. Two of its assumptions were often invalid: food was unlikely to be limiting in four of five populations, and sexual biomass production accelerated, not decelerated, with colony size in three of five populations. One of five Pheidole populations studied had higher caste ratios (soldiers /workers) in reproductive colonies as predicted, and in no species did caste functions conform to predictions. We also adapted three models from plant defense theory to study between-species patterns of caste allocation. Among 12 litter Pheidole the amount of sterile biomass devoted to soldiers varied from 18 to 62%. Queen size, growth rate, and soldier investment positively covaried. Only one model, the cost of replacement hypothesis (McKey 1979), correctly predicted that species with costly female alates invest more in defense. The two hypotheses linking apparency to defense may also be valid if fast-growing colonies are more likely to attract the attention of predators.     

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

Summary 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.     

Polyandry in the genus Apis, particularly Apis andreniformis

Using four polymorphic microsatellite loci, we found that four Apis andreniformis queens collected in Thailand each mated at least 10–20 times, producing an average relatedness, g _ww, of workers of 0.30 ± 0.007, and an average effective number of matings of 9.1 ± 2.2. The degrees of polyandry and intra-colonial genetic relatedness in A. andreniformis are similar to those in A. mellifera, slightly more than in A. florea, and up to 6 times less than in A. dorsata. We argue that while presently favoured hypotheses for the evolution of polyandry in monogynous social insects may adequately explain the evolution of up to five or six matings, they are inadequate to explain the extreme polyandry (10–60 matings) observed in Apis. One alternative possibility is that colony fitness is a non-additive function of the fitness of individual subfamilies. Such behavioral over-dominance may mean that queen fitness is increased by high levels of polyandry, which increase the probability of desirable combinations of worker genotypes occurring in one colony. The special attributes of honey bees which may lead to behavioral over-dominance include colony aggregation (which may increase the incidence of disease), and frequent long-distance migration. Received: 8 May 1996/Accepted after revision: 9 August 1996     

Phenotypic plasticity and “cultural transmission” of alternative social organizations in the fire ant Solenopsis invicta

Summary We investigated the process of sexual maturation in winged queens of the fire ant Solenopsis invicta, a species with two distinct forms of social organization. We found that queens of the monogynous social form (single reproductive queen per colony) differ little or not at all from queens of the polygynous form (multiple reproductive queens per colony) in weight and fat content when these are pupae or newly-eclosed adults. Furthermore, the size of a sclerotized region of the adult thorax, which is set during larval growth, does not differ between queens of the two forms. In contrast, winged queens of the two social forms differ dramatically in their physiological phenotypes once they have matured, with monogynous queens weighing more and having greater fat reserves than polygynous queens. A crossfostering experiment revealed that the different maturation processes of queens of the two forms are induced largely by the type of colony in which a queen matures (monogynous or polygynous) rather than being due to intrinsic genetic differences between the forms. However, genetic variation at a single locus does appear to play some role in determining physiological phenotype in queens of the polygynous form, providing an example of genotype-environment interaction in the expression of these physiological traits. Differences between the social forms in the mature phenotypes that are produced constrain the reproductive options of queens, so that the characteristic social organization of a colony is perpetuated by virtue of the social environment in which new queens are reared. Correspondence to: L. Keller     

Facultative polyandry and the role of infant-carrying in wild saddle-back tamarins (Saguinus fuscicollis)

Summary Wild saddle-back tamarins (Saguinus fuscicollis) in southeastern Peru have a variable mating system that can differ both between territories at any one time and within territories over time. Groups are usually monogamous or cooperatively polyandrous, but are occasionally even polygynous. This study addressed the following questions: why does this population contain both monogamous and polyandrous groups simultaneously? What factors determine whether specific groups are monogamous or polyandrous? The data from this study population tentatively support the hypothesis that adults should mate monogramously only if they have nonreproductive helpers (usually older offspring) to help rear infants. Without helpers, the reproductive success of both males and females is hypothesized to be higher, on average, if they mate polyandrously than if they mate monogamously. The proposed benefits of polyandry to males and females differ quantitatively, but in both cases benefits stem from the help that males provide in rearing young. The following results support this hypothesis. (1) Lone pairs were never seen to attempt breeding, and calculations suggest that the costs of lactation and infant-carrying are too great for lone pairs to have a high probability of being able to raise twin offspring (the normal litter size). (2) Polyandrous males and nonreproductive offspring contributed substantially to infant care, particularly infant-carrying (fig. 2). (3) Adult males carried infants approximately twice as often as did lactating females, presumably because of the combined costs of (a) lactation (Fig. 3) and (b) infant-carrying (Fig. 4). The proximate causes of cooperative polyandry inS. fuscicollis appear to be different from those responsible in several bird species, showing that cooperative polyandry is a complex phenomenon.