Investment Sex Ratio Research Articles

Colony developmental patterns in different local populations of the Turkish bumble bee, Bombus terrestris dalmatinus

SUMMARYAs a preliminary to the use of bumble bee colonies in greenhouse pollination in Turkey, research was initiated on the relevant characteristics of the native bumble bee Bombus terrestris dalmatinus. The same methodology was used that has been successful in the rearing of B. t. terrestris colonies. Queens were collected in four coastal localities (Bodrum, Antalya, Alata and Adana) and characterized by the different dates of the young queen's emergence from diapause. This emergence varied from the end of November to February. Despite the variation in collecting dates, the patterns of development of the colonies produced were similar, indicating that, in this respect, no ecotypes existed. As in B. t. terrestris, the relative timing of the switch point, i.e. when mainly haploid eggs are laid by the queen, is the determining factor for the number of workers and the investment sex ratio of the B. t. dalmatinus colonies. The colonies of these two subspecies develop according to the same principles. The colonies from all four regions had, on average, a male-biased investment sex ratio (0.21, queen fraction), which is a common feature for bumble bees. On the basis of the number of workers produced (c. 150 workers), the colonies from these four Turkish areas are very well suited for pollination purposes.

COLONY SEX RATIOS, CONFLICT BETWEEN QUEENS AND WORKERS, AND APPARENT QUEEN CONTROL IN THE ANT PHEIDOLE DESERTORUM.

Sex-ratio conflict between queens and workers was explored in a study of colony sex ratios, relatedness, and population investment in the ant Pheidole desertorum. Colony reproductive broods consist of only females, only males, or have a sex ratio that is extremely male biased. Colonies producing females (female specialists) and colonies producing males (male specialists) occur at near equal frequency in the population. Most colonies apparently specialize in producing one reproductive sex throughout their life. Allozyme analyses show that relatedness does not differ within male-specialist and female-specialist colonies and they do not appear to differ in available resources. In the population, workers are nearly three times more closely related to females than males; however, the investment sex ratio is near equal (1.01, female/male), which is consistent with queen control. Selection should be strong on workers to increase investment in reproductive females, so why do workers in male-specialist colonies produce only (or nearly only) males? One hypothesis is that queens in male-specialist colonies prevent the occurrence of reproductive females, perhaps by producing worker-biased female eggs. An earlier simulation study of genetic evolution of sex ratios in social Hymenoptera (Pamilo 1982b) predicts that such mechanisms can result in the evolution of bimodal colony sex ratios and queen control. Results on P. desertorum are generally consistent with that study; however, information is not currently available to test some of the model's predictions and assumptions.

Sex allocation in a facultatively polygynous ant: between-population and between-colony variation

We investigated sex allocation in three U.K. populations of the facultatively polygynous ant Leptothorax acervorum over 1–3 years. The first main finding was that, across sites, the population sex-investment ratio changed from significantly female biased to significantly male biased with increasing polygyny. This was consistent with workers controlling sex allocation and reacting to changes in their population-level relatedness asymmetry. It was also consistent with local resource competition due to reproduction by colony budding under polygyny. Worker control was supported by the finding that queen number had no effect on sex allocation among polygynous colonies. The second main result was that monogynous colonies consistently produced more female-biased sex-investment ratios than polygynous colonies in one site only (Santon). The results from Santon supported both the relative relatedness asymmetry hypothesis and the idea of sex ratio compensation due to colony budding. The workers’ response to their population-level relatedness asymmetry reinforced the case for relatedness asymmetry being influential at the colony level. The other populations could have lacked split sex ratios because polygynous colonies were either comparatively rare or common, making them behave as almost entirely monogynous (Aberfoyle) or polygynous (Roydon) populations. In Roydon, this was consistent with the inference from allozyme data that monogynous and polygynous colonies did not differ in their worker relatedness asymmetries. The final principal finding was that, of hypotheses linking the colony sex-investment ratio with sexual productivity, there was support for the constant female hypothesis but not for the constant male, cost variation, or multifaceted parental investment hypotheses.

Testing kin selection with sex allocation data in eusocial hymenoptera

Sex allocation data in eusocial Hymenoptera (ants, bees and wasps) provide an excellent opportunity to assess the effectiveness of kin selection, because queens and workers differ in their relatedness to females and males. The first studies on sex allocation in eusocial Hymenoptera compared population sex investment ratios across species. Female-biased investment in monogyne (= with single-queen colonies) populations of ants suggested that workers manipulate sex allocation according to their higher relatedness to females than males (relatedness asymmetry). However, several factors may confound these comparisons across species. First, variation in relatedness asymmetry is typically associated with major changes in breeding system and life history that may also affect sex allocation. Secondly, the relative cost of females and males is difficult to estimate across sexually dimorphic taxa, such as ants. Thirdly, each species in the comparison may not represent an independent data point, because of phylogenetic relationships among species. Recently, stronger evidence that workers control sex allocation has been provided by intraspecific studies of sex ratio variation across colonies. In several species of eusocial Hymenoptera, colonies with high relatedness asymmetry produced mostly females, in contrast to colonies with low relatedness asymmetry which produced mostly males. Additional signs of worker control were found by investigating proximate mechanisms of sex ratio manipulation in ants and wasps. However, worker control is not always effective, and further manipulative experiments will be needed to disentangle the multiple evolutionary factors and processes affecting sex allocation in eusocial Hymenoptera.

Bumblebee sex ratios: why do bumblebees produce so many males?

Sex investment ratios in populations of bumblebees are male biased, which contradicts theoretical predictions. Male-biased investment ratios in eusocial Hymenoptera are assumed to be non-stable for both the queen and her workers. In this paper, we show that male-biased sex allocation does not necessarily decrease fitness in the bumblebee Bombus terrestris. A male-biased investment ratio can be the result of an optimal allocation of resources when resources are scarce if (i) there is a large cost difference between male and female production, (ii) there is uncertainty about the amount of resources a colony can invest, and (iii) only a proportion of the investment made in an individual can be reused. This resource allocation then leads to split sex ratios depending on the amount of resources available to a bumblebee colony: colonies under low resource conditions will show a male-biased investment ratio, whereas colonies under high resource conditions allocate more resources towards females. However, the extent to which bumblebee populations show a male-biased sex allocation cannot be explained by cost differences between male and female production alone. In a recent paper, A. F. G. Bourke argued that male-biased investment ratios in bumblebee populations are a by-product of the occurrence of protandry (males emerge before females). Here we will extend Bourke's argument and show that within a protandrous population, both protandrous and protogynous (females emerge before males) colonies exist. The existence of protandrous and protogynous colonies results in split sex ratios in time, because protogynous colonies rely on males produced by protandrous colonies (partial protandry).

Sex ratios in bumble bees

The median proportion of investment in females among 11 populations of seven bumble bee (Bombus) species was 0.32 (range 0.07 to 0.64). By contrast, two species of workerless social parasites in the related genusPsithyrushad female–biased sex allocation, the reasons for which remain unclear. Male–biased sex allocation inBombuscontradicts the predictions of Trivers and Hare's sex ratio model for the social Hymenoptera, which are that the population sex investment ratio should be 0.5 (1:1) under queen control and 0.75 (3:1 females:males) under worker control (assuming single, once–mated, outbred queens and non–reproductive workers). Male bias inBombusdoes not appear to be either an artefact, or purely the result of symbiotic sex ratio distorters. According to modifications of the Trivers—Hare model, the level of worker male–production inBombusis insufficient to account for observed levels of male bias. There is also no evidence that male bias arises from either local resource competition (related females compete for resources) or local mate enhancement (related males cooperate in securing mates). Bulmer presented models predicting sexual selection for protandry (males are produced before females) in annual social Hymenoptera and, as a consequence (given some parameter values), male–biased sex allocation. Bumble bees fit the assumptions of Bulmer's models and are protandrous. These models therefore represent the best current explanation for the bees' male–biased sex investment ratios. This conclusion suggests that the relative timing of the production of the sexes strongly influences sex allocation in the social Hymenoptera.

Sex ratios, local fitness enhancement and eusociality in the allodapine bee Exoneura richardsoni

Previous studies of a facultatively eusocial allodapine bee, Exoneura richardsoni Rayment, indicated that high levels of cooperative nesting among close relatives seem to be maintained by benefits that lead to increases in per capita brood production. These traits could lead to local fitness enhancement, which in turn could select for female-biased sex ratios. We show here that sex investment ratios in this species are female-biased in small colony sizes, becoming progressively male-biased in larger colonies, consistent with expectations for local fitness enhancement, but not explainable by alternative models. Our results support previous suggestions that local fitness enhancement can lead to sex ratio bias in primitively social Hymenoptera, but differ from previous studies by suggesting that patterns of bias could lower selective thresholds for sib-directed altruism in small colonies, but have an opposing effect in large colonies.

Sex–ratio regulation: the economics of fratricide in ants

In many insect societies, workers can manipulate the reproductive output of their colony by killing kin of lesser value to them. For instance, workers of the mound-building Formica exsecta eliminate male brood in colonies headed by a single-mated queen. By combining an inclusive fitness model and empirical data, we investigated the selective causes underlying these fratricides. Our model examines until which threshold stage in male brood development do the workers benefit from eliminating males to rear extra females instead. We then determined the minimal developmental stage reached by male larvae before elimination in F. exsecta field colonies. Surprisingly, many male larvae were kept until they were close to pupation, and only then eliminated. According to our model, part of the eliminated males were so large that workers would not benefit from replacing them with new females. Moreover, males were eliminated late in the season, so that new females could no longer be initiated, because matings take place synchronously during a short period. Together, these results indicate that workers did not replace male brood with new females, but rather reduced total brood size during late larval development. Male destruction was probably triggered by resource limitation, and the timing of brood elimination suggests that males may have been fed to females when these start to grow exponentially during the final larval stage. Hence, the evolution of fratricides in ants is best explained by a combination of ecological, demographic and genetic parameters.

Sex investment ratios in monogyne and polygyne populations of the fire ant Solenopsis invicta

AbstractBoth monogyne (single queen per colony) and polygyne (multiple queens per colony) populations of the fire ant Solenopsis invicta are good subjects for tests of kin selection theory because their genetic and reproductive attributes are well‐characterized, permitting quantitative predictions about the degree to which sex investment ratios should be female‐biased if workers and not queens control reproductive allocation. In the study populations, an investment ratio of 3 females: 1 male is predicted (a proportional investment in females of 0.75) in the monogyne form, whereas a proportional investment in females between 0.637 and 0.740 is expected in the polygyne form. To test these predictions, colonies from a single population of each social form were collected and censused during three different seasons. Consistent with their alternative modes of colony founding, monogyne colonies invested more in reproduction (sexual production) and less in growth/maintenance (worker production) than did the polygyne colonies. Overall, the sex investment ratios were female‐biased in both forms, although there was considerable seasonal variation. After adjusting for sex‐specific energetic costs, the proportional investment in females was 0.607 in the monogyne population, a value in between those expected under complete control by either the queen or the workers. However, when combined with data from four other previously studied monogyne populations in the U.S.A., the mean investment ratio did not differ significantly from the value predicted if workers have exclusive control. In the polygyne population, the proportional investment in females of 0.616 was consistent with the level of female bias expected under partial to complete worker control, although the potential influence of two confounding factors — possible contact with monogyne colonies and the preponderance of sterile diploid males — weakens this conclusion somewhat. Taken as a whole, the sex investment ratios of monogyne and polygyne populations of S. invicta are consistent with at least partial worker control. Of several ultimate and proximate explanations that have been proposed to explain inter‐colonial variation in the sex investment ratio, only the effect of the primary sex ratio (female‐determined eggs: male‐determined eggs) laid by the queen appears to account for the observed variation among monogyne colonies. In the polygyne population, there is limited support for the hypothesis that greater resource abundance favors investment in females.

Primary and secondary sex ratios in monogyne colonies of the fire ant

Patterns of sex ratios and sex investment ratios play an instrumental role in theoretical and empirical considerations of the evolution and maintenance of insect sociality. An assumption of sex-ratio studies in the eusocial Hymenoptera is that workers, who reproduce indirectly by rearing the queen's offspring, have the ability to distinguish the sex of larvae and direct preferential treatment towards developing females. To determine if workers of the monogyne (single queen per colony) form of the fire ant, Solenopsis invicta, have this ability and the extent to which they might use it to influence the sex ratio of the colony's reproductives, the primary sex ratio (ratio of male/female-determined eggs produced by the queen) and the secondary sex ratio (ratio of male/female reproductive adults or pupae) were compared, in mature colonies producing sexuals of almost exclusively one sex or the other, a common condition in monogyne colonies of this and other ant species. Queens of male-producing colonies laid about 19% haploid (male) eggs, whereas queens of female-producing colonies laid about 11% haploid eggs. In both cases, the proportion of haploid eggs laid was far higher than the proportion of adult males reared by the workers. These results suggest that workers strongly influence the colony's secondary sex ratio by selective elimination of male larvae, but the magnitude of this influence depends upon the primary sex ratio produced by the queen. Highly male-biased secondary sex ratios produced by workers in relation to more male-biased primary sex ratios may be caused by ergonomic constraints that could limit the ability of workers to skew the sex-investment ratio.

Sexual Size Dimorphism and Sex Ratios in Bees and Wasps

When parental investment is estimated from the body weight of offspring, the sex investment ratio increases with increasing sexual size dimorphism across species of bees and wasps. This relationship was recently found in ants and was hypothesized to be artifactual and occur because body weight overestimates parental investment in the larger sex (females) proportional to the degree they are larger than the smaller sex (males). Analyses using an apparently unbiased alternative to body weight in estimating parental investment in solitary wasps support this hypothesis. The analyses also show, however, that increase in the sex investment ratio with increasing sexual size dimorphism may not be entirely artifactual. In solitary wasps, it is hypothesized that actual covariance between sexual size dimorphism and the sex investment ratio will occur if mothers produce small males when those males compete primarily with brothers for access to mates.

Colony structure of a bamboo-dwellingTetraponera sp. (Hymenoptera: Formicidae: Pseudomyrmecinae) from Malaysia

The colony structure of the bamboo-inhabiting SE-Asian pseudomyrmecine antTetraponera sp. PSW-80 nearattenuata F. Smith was investigated at the Ulu Gombak Field Studies Centre, Selangor, West-Malaysia. Based on the dissection of 54 stem internodes from 12 different culms of the large bambooGigantochloa scortechinii Gamble and on the mapping of three colonies, the following demographic characteristics emerge. The colonies are monogynous but highly polydomous (at least up to 36 internodes and up to 9 stems occupied) and very populous for a pseudomyrmecine not involved in an ant-plant mutualism. One completely censused colony had 6953 adult workers and 2079 alates (adults plus pupae). The single queen suppresses gyne development in her own “nest” and, to a lesser extent, in other “nests” within the same stem. The overall numerical sex ratio was 0.96∶1 (females:males), the investment sex ratio, 2.93∶1, i.e., almost exactly the 3∶1 ratio expected for a monogynous outbred hymenopteran in which the colony queen also produces all the male offspring. Brood is distributed to all other nest chambers from the queenright chamber. The symbiotic pseudococcids (Kermicus wroughtoni Newstead) are present in all inhabited internodes, with small early instar individuals prevailing numerically by far over the larger stages. The rieht well secluded honeydew supply within the internode and the efficient architectural protection provided by the internode wall (access usually only through a 2 × 3 mm-hole) allowT. sp. PSW-80 to reach an unusually large colony size without being an aggressive and protective plant mutualist like other members of its subfamily with similar demographic features.

Relatedness and sex ratio in a primitively eusocial halictine bee

Lasioglossum laevissimum was studied in Calgary, Alberta, where it is eusocial with one worker brood. Estimates of relatedness were obtained among various categories of nestmate based upon four polymorphic enzyme loci, two of which exhibited significant levels of linkage disequilibrium. Relatedness estimates among workers and among reproductive brood females were very close to the expected 0.75 value that obtains when nests are headed by one, singly mated queen. However, relatedness between workers and the reproductive brood females they reared was significantly lower than 0.75. A low frequency of orphaning with subsequent monopolisation of oviposition by one worker brood female in orphaned nests may explain these results. Workers were significantly more and queens significantly less closely related to male reproductives than expected if all males were to have resulted from queen-laid eggs. Orphaning and worker-produced males contribute to this result. The sex investment ratio was 1:2.2 in favour of females, in excellent agreement with the predictions based upon relative relatednesses between workers and reproductive brood males and females. Adaptive intercolony variation in investment ratios was detected: the sex ratio was more heavily female-biased in nests in which the relative relatedness asymmetry between workers and reproductive brood was more female-biased. The study species is the most weakly eusocial hymenopteran for which relatedness estimates and sex ratio data are available. With high relatedness among nestmates and a strongly female-biased sex ratio, this study suggests the importance of indirect fitness contributions in the early stages of social evolution.

Biology of Calliopsis pugionis (Hymenoptera: Andrenidae): Nesting, Foraging, and Investment Sex Ratio

Calliopsis pugionis Cockerell usually nests in dense aggregations, with up to 1,650 nests per m2, in areas of bare soil. A female provisions one cell each day with pollen from composites, here Encelia and Hemizonia, usually in three or four pollen foraging trips, followed by a trip in which she collects nectar and pollen for her own consumption. Matings take place both on flowers and at nest sites. Males compose 70.8% of the larvae provisioned. Investment sex ratio (M/F) ranges from 1.07 to 2.43 when estimated from several measures of cost, including adult dry weight, prepupal wet weight, meconia weight, pollen trip foraging time, total foraging time, and number of days. The best estimate of investment sex ratio is probably about 2. Quantitative predictions of effect on sex ratio of differential parasitism of males and females by a cleptoparasitic bee, Holcopasites ruthae Cooper, are derived. These account for only some of the male bias in investment sex ratio; other factors could include local resource competition.

Worker reproduction and related behavior in orphan colonies of a Japanese paper wasp,Polistes jadwigae (Hymenoptera, Vespidae)

Worker reproduction and related behavior in 2 orphan colonies ofPolistes jadwigae, one of which had been maintained by a queen and 5 artificially introduced alien workers, were observed. After the queen loss, a dominance hierarchy was established among workers, and several workers laid eggs without physical interference from other workers. Only males emerged from worker-laid eggs, however, a few new queens were produced from queen-laid eggs. Investment sex ratio of queenright (=normal) colonies (0.27) fell between the 2 theoretical values, corresponding to worker control (0.20 or 0.18) and queen control (0.48 or 0.46) of the sex ratio, both being calculated by considering the excess of males produced in the orphan colonies.

Haplodiploidy and the Evolution of Facultative Sex Ratios in a Primitively Eusocial Bee

In eusocial Hymenoptera, the haplodiploid system of sex determination creates relatedness asymmetries such that workers are more closely related on average to their sisters than to their brothers. For such societies, kin-selection theory and sex-ratio theory predict that workers maximize their inclusive fitness by biasing the investment sex ratio toward females. To test the prediction of sex-ratio biasing, relatedness asymmetries were experimentally manipulated in colonies of the primitively eusocial bee Augochlorella striata (Halictidae: Hymenoptera) by removing or not removing foundress queens. Queenright colonies (relatedness asymmetry present) produced a more female-biased sex ratio than did queenless colonies (relatedness asymmetry absent). Worker reproduction and unmated replacement queens can be discounted as alternative explanations. Workers therefore facultatively adjusted their colony's sex ratio and, in the presence of a relatedness asymmetry, biased the investment sex ratio toward their more closely related sisters and away from their more distantly related brothers.

Population Genetic Structure and Social Evolution in the Sphecid Wasp Microstigmus comes

Genetic structure and sex allocation were studied in a natural population of the primitively eusocial sphecid wasp Microstigmus comes. No higher-level genetic structure was discernible at the level of the subpopulation, and microgeographic structure at the level of the local deme or individual host palm was, at most, modest. In contrast, genetic structure at the level of the individual nest was striking, with the average genetic relatedness among female nest mates estimated to be 0.62-0.67. This high relatedness results from the fact that colonies comprise relatively simple families, which are, in many instances, matrifilial monogynous societies. High relatedness among female nest mates and the absence of conspicuous higher-level structure, in conjunction with the observed female-biased sexinvestment ratios, are compatible with the interpretation that kin selection has played a major role in the origin of eusocial behavior in the recent ancestors of this wasp. The inferred colony composition and social organization further suggest that this social evolution may have occurred via a subsocial route, with simple matrifilial families rather than polygynous groups serving as the principal setting for the development of worker altruism.

Comparative Analysis of Sex-Investment Ratios in Slave-Making Ants

Comparative Analysis of Sex-Investment Ratios in Slave-Making Ants

Sex-Investment Ratios in Ants: Has Female Bias Been Systematically Overestimated?

The claim by Trivers and Hare (1976) and Nonacs (1986a) that the ratio of sexual investment in monogynous ants is as much female-biased as 3:1 on the average is argued to be untenable because of (1) bias in the gyne-to-male dry-weight cost ratios, as a result of increasingly diverging rates of respiration and fat accumulation with increasing sexual dimorphism; and (2) bias in the numerical sex ratios estimated from small samples. Partial regressions of the numerical gyne-to-male (f/m) sex ratio (S) on the individual dry-weight ratio (D) and sample size (N) appeared to be consistently present in the data sets for monogynous and polygynous ants, although significantly so only for the monogynous ants. These relationships were primarily interpreted as methodological artifacts, but possible biological explanations are also discussed. The alternative explanations, however, are less well supported by data and/or apply to only parts of the data set. Under the assumption that dry-weight cost ratios are unbiased only for species without sexual dimorphism, an approximate formula was derived to transfer dry-weight f/m cost ratios (D) into approximately energetic f/m cost ratios (C). The formula C = D0.7 was found to give a reliable quantitative prediction of the difference between the individual dry-weight ratio and the energetic-cost ratio in Lasius niger, which was earlier estimated empirically (Boomsma and Isaaks 1985). After adjustment for the assumed artifacts, the geometric-mean investment ratio across monogynous ants was estimated to be 1.82:1 in favor of gynes and to differ significantly from both 1:1 and 3:1. The adjusted pattern is consistent with the hypothesis that workers control the sex-allocation process throughout monogynous ants, but in a context of variable degrees of relatedness asymmetry because of the frequent occurrence of multiple mating and worker reproduction.

Sex-Investment Ratios and relatedness in the Monogynous Ant Lasius niger (L.)

Sex-Investment Ratios and relatedness in the Monogynous Ant Lasius niger (L.)