Reproductive allocation within a polygyne, polydomous colony of the ant Myrmica rubra

1. Ant colonies commonly have multiple egg‐laying queens (secondary polygyny). Polygyny is frequently associated with polydomy (single colonies occupy multiple nest sites) and restricted dispersal of females. The production dynamics and reproductive allocation patterns within a population comprising one polygyne, polydomous colony of the red ant Myrmica rubra were studied. 2. Queen number per nest increased with nest density and the number of adult workers increased with the number of resident queens and with nest density. This suggests that nest site limitation promotes polygyny and that workers accumulate in nest units incapable of budding. 3. Nest productivity increased with the number of adult workers and production per queen was independent of queen number. Productivity increased with nest density, suggesting local resource enhancement. This shows that productivity can be a linear function of queen numbers and that the limiting factor is not the egg‐laying capacity of queens. 4. The total and per capita production of reproductives decreased towards the periphery of the colony, suggesting that the spatial location of nest units affects sexual production. Thus nests at the periphery of the colony invested more heavily in new workers. This is consistent with earlier observations in plants and could either represent investment in future budding or increased defence. 5. The colony produced only five new queens and 2071 males, hence the sex ratio was extremely male biased.     

Ecology, life history and resource allocation in the ant, Leptothorax nylanderi

We aimed at identifying the causal basis of previously shown interrelations between demographic and genetic colony structure, ecological factors and split sex ratios in the ant, Leptothorax nylanderi. Colony-level variation in sex allocation was only partly explained by annual fluctuations during eight study years and by resource availability as indicated by sexual production of colonies. Allocation ratios were highly male-biased in dense populations with ephemeral nest sites and high frequencies of colonies containing several unrelated matrilines. Field observations and experimental manipulations showed that nest site limitation leads to such heterogeneous colonies. Laboratory experiments demonstrated that genetic heterogeneity directly causes male-biased investment, although relatedness asymmetry is not influenced by invasion of unrelated queens. The influence of genetic composition on allocation strategies might either be explained by negative feedback mechanisms connected with habitat saturation or by a lower efficiency of heterogeneous colonies. Our results thus demonstrate which factors other than variation in relatedness asymmetry can explain split sex ratios in ants. An empirical test of a model on reproductive allocation revealed on-going queen-worker conflict over colony growth and sexual reproduction. Workers controlled reproductive allocation, but queen-worker conflict ceased in large colonies with a high survival rate.     

Resource allocation in a social wasp: effects of breeding system and life cycle on reproductive decisions

Organisms must make important decisions on how to allocate resources to reproduction. We investigated allocation decisions in the social wasp Vespula maculifrons to understand how social insects make reproductive choices. We first determined how annual colonies apportioned resources to growth and reproduction by analysing developing brood. In contrast to expectations, colonies invested in both growth (workers) and reproduction (males) simultaneously. In addition, colonies showed evidence of producing males in pulses and reversing their reproductive choices by decreasing investment in males late in the season. This reversal is consistent with theory suggesting that colonies decrease production in males if fitness of late emerging males is low. To further investigate reproductive decisions within colonies, we determined if the male mates of multiply-mated queens varied in their reproductive success over time. Sperm use by queens did vary over time suggesting that male success may depend on sperm clumping within the female reproductive tract. Finally, we tested if colony sex ratio conformed to expectations under kin selection theory that nestmate relatedness would positively correlate with investment in new queens if workers controlled sex allocation. Surprisingly, the proportion of queens produced by colonies was negatively correlated with nestmate relatedness, suggesting that allocation may be shaped by advantages arising from increased genetic diversity resulting from multiple mating by queens. Overall, our study suggests that the reproductive decisions of colonies are flexible and may depend both on environmental cues arising from energetic needs of the colony and genetic cues arising from mating behaviours of queens.     

Density-dependent dispersal promotes female-biased sex allocation in viscous populations

A surprising result emerging from the theory of sex allocation is that the optimal sex ratio is predicted to be completely independent of the rate of dispersal. This striking invariance result has stimulated a huge amount of theoretical and empirical attention in the social evolution literature. However, this sex-allocation invariant has been derived under the assumption that an individual''s dispersal behaviour is not modulated by population density. Here, we investigate how density-dependent dispersal shapes patterns of sex allocation in a viscous-population setting. Specifically, we find that if individuals are able to adjust their dispersal behaviour according to local population density, then they are favoured to do so, and this drives the evolution of female-biased sex allocation. This result obtains because, whereas under density-independent dispersal, population viscosity is associated not only with higher relatedness—which promotes female bias—but also with higher kin competition—which inhibits female bias—under density-dependent dispersal, the kin-competition consequences of a female-biased sex ratio are entirely abolished. We derive analytical results for the full range of group sizes and costs of dispersal, under haploid, diploid and haplodiploid modes of inheritance. These results show that population viscosity promotes female-biased sex ratios in the context of density-dependent dispersal.     

Budding dispersal and the sex ratio

There is much interest in understanding how population demography impacts upon social evolution. Here, we consider the impact of rate and pattern of dispersal upon a classic social evolutionary trait--the sex ratio. We recover existing analytical results for individual dispersal, and we extend these to allow for budding dispersal. In particular, while a cancelling of relatedness and kin competition effects means that the sex ratio is unaffected by the rate of individual dispersal, we find that a decoupling of relatedness and kin competition means that budding dispersal favours increasingly female-biased sex ratios. More generally, our analysis illustrates the relative ease with which biological problems involving class structure can be solved using a kin selection approach to social evolution theory.     

Significant reproductive skew in the facultatively polygynous ant Pheidole pallidula

Reproductive skew - the extent to which reproduction is unevenly shared between individuals in a social group - varies greatly between and within animal species. In this study, we investigated how queens share parentage in polygynous (multiple queen) colonies of the Mediterranean ant Pheidole pallidula. We used highly polymorphic microsatellites markers to determine parentage of gynes (new queens), males and workers in P. pallidula field colonies. The comparison of the genotypes of young and adult workers revealed a very low queen turnover (less than 2%). The first main finding of the study of reproductive skew in these colonies was that there was a significant departure from equal contribution of queens to gyne, male and worker production. Reproductive skew was greater for male production than for queen and worker production. There was no relationship between the magnitude of the reproductive skew and the number of reproductive queens per colony, their relatedness and the overall colony productivity, some of the factors predicted to influence the extent of reproductive skew. Finally, our study revealed for the first time a trade-off in the relative contribution of nestmate queens to gyne and worker production. The queens contributing more to gyne production contributed significantly less to worker production.     

Patterns of resource allocation in the dioecious alpine herb Aciphylla simplicifolia (Apiaceae)

Abstract Patterns of reproductive and vegetative biomass allocation were compared in male and female plants of the alpine herb Aciphylla simplicifolia. Male and female plants had similar vegetative biomass but differed in the pattern of resource allocation. Inflorescences of males and females were similar in weight at the time of flowering, but differed in biomass allocation to some structures within the inflorescences, particularly those associated with ovule production and pollinator attraction (number and size of flowers). At the time of fruit production, female inflorescences were 2.6 times heavier than at flowering with developing fruit six times heavier than flowers. In addition to the increase in biomass allocated to structures associated with the provisioning and dissemination of seed, support structures (main and side stalks) were also heavier. As a result of this additional investment of resources at the time of fruit production, the reproductive effort (RE) of female plants was much higher than that of males: 37% of above ground biomass compared with 21% for males. Differences in RE did not change with plant size; however, allocation to reproduction appeared to be a constant proportion of biomass over nearly all plant sizes sampled. These results show that sex‐specific resource allocation can be a complex of temporal and morphological patterns.     

Size‐dependent sex allocation in a simultaneous hermaphrodite parasite

Most models of sex allocation distinguish between sequential and simultaneous hermaphrodites, although an intermediate sexual pattern, size‐dependent sex allocation, is widespread in plants. Here we investigated sex allocation in a simultaneous hermaphrodite animal, the tapeworm Schistocephalus solidus, in which adult size is highly variable. Sex allocation was determined using stereological techniques, which allow measuring somatic and reproductive tissues in a common currency, namely volume. We investigated the relationships between individual volume and allocation to different reproductive tissues using an allometric model. One measure of female allocation, yolk gland volume, increased more than proportionally with individual volume. This is in contrast to the measure of male allocation, testis volume, which showed a strong tendency to increase less than proportionally with individual volume. Together these patterns led to sex allocation being strongly related to individual volume, with large individuals being more biased towards female allocation. We discuss these findings in the light of current ideas about size‐dependent sex allocation in, primarily, plants and try to extend them to simultaneous hermaphrodite animals.     

Kin discrimination and sex ratios in a parasitoid wasp

Sex ratio theory provides a clear and simple way to test if nonsocial haplodiploid wasps can discriminate between kin and nonkin. Specifically, if females can discriminate siblings from nonrelatives, then they are expected to produce a higher proportion of daughters if they mate with a sibling. This prediction arises because in haplodiploids, inbreeding (sib-mating) causes a mother to be relatively more related to her daughters than her sons. Here we formally model this prediction for when multiple females lay eggs in a patch, and test it with the parasitoid wasp Nasonia vitripennis. Our results show that females do not adjust their sex ratio behaviour dependent upon whether they mate with a sibling or nonrelative, in response to either direct genetic or a range of indirect environmental cues. This suggests that females of N. vitripennis cannot discriminate between kin and nonkin. The implications of our results for the understanding of sex ratio and social evolution are discussed.     

Reproductive conflicts in polyandrous and polygynous ant Formica sanguinea

The occurrence of multiple reproductives within an ant colony changes the balance between indirect fitness benefits and reproductive competition. We test whether the number of matings by an ant queen (polyandry) correlates negatively with the number of reproductive queens in the colony (polygyny), whether the patrilines and matrilines differ in their contribution to the sexual and worker progeny and whether there is an overall reproductive skew. For these aims, we genotyped both worker and sexual offspring from colonies of the ant Formica sanguinea in three populations. Most colonies were monogynous, but eight (11%) were polygynous with closely related queens. Most queens in the monogynous colonies (86%) had mated with multiple males. The effective paternity was lower than the actual number of mates, and the paternity skew was significant. Furthermore, in some monogynous colonies, the patrilines were differently represented in the worker pupae and sexual pupae produced at the same time. Likewise, the matrilines in polygynous colonies were differently present in worker pupae and male offspring. The effective number of matings by a queen was significantly lower in polygynous colonies (mean m_e = 1.68) than in monogynous colonies (means 2.06–2.61). The results give support to the hypotheses that polyandry and polygyny are alternative breeding strategies and that reproductive competition can lead to different representation of patrilines and matrilines among the sexual and worker broods.     

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

We investigated sex allocation in three U.K. populations ofthe facultatively polygynous ant Leptothorax acervorum over1-3 years. The first main finding was that, across sites, thepopulation sex-investment ratio changed from significantly femalebiased to significantly male biased with increasing polygyny.This was consistent with workers controlling sex allocationand reacting to changes in their population-level relatedness asymmetry.It was also consistent with local resource competition due to reproductionby colony budding under polygyny. Worker control was supportedby the finding that queen number had no effect on sex allocationamong polygynous colonies. The second main result was that monogynouscolonies consistently produced more female-biased sex-investmentratios than polygynous colonies in one site only (Santon). Theresults from Santon supported both the relative relatednessasymmetry hypothesis and the idea of sex ratio compensationdue to colony budding. The workers' response to their population-levelrelatedness asymmetry reinforced the case for relatedness asymmetrybeing influential at the colony level. The other populationscould have lacked split sex ratios because polygynous colonieswere either comparatively rare or common, making them behaveas almost entirely monogynous (Aberfoyle) or polygynous (Roydon) populations.In Roydon, this was consistent with the inference from allozyme datathat monogynous and polygynous colonies did not differ in theirworker relatedness asymmetries. The final principal findingwas that, of hypotheses linking the colony sex-investment ratiowith sexual productivity, there was support for the constantfemale hypothesis but not for the constant male, cost variation,or multifaceted parental investment hypotheses.     

Multiple breeders, breeder shifts and inclusive fitness returns in an ant

In social insects, colonies may contain multiple reproductively active queens. This leads to potential conflicts over the apportionment of brood maternity, especially with respect to the production of reproductive offspring. We investigated reproductive partitioning in offspring females (gynes) and workers in the ant Formica fusca, and combined this information with data on the genetic returns gained by workers. Our results provide the first evidence that differential reproductive partitioning among breeders can enhance the inclusive fitness returns for sterile individuals that tend non-descendant offspring. Two aspects of reproductive partitioning contribute to this outcome. First, significantly fewer mother queens contribute to gyne (new reproductive females) than to worker brood, such that relatedness increases from worker to gyne brood. Second, and more importantly, adult workers were significantly more related to the reproductive brood raised by the colony, than to the contemporary worker brood. Thus, the observed breeder shift leads to genetic benefits for the adult workers that tend the brood. Our results also have repercussions for genetic population analyses. Given the observed pattern of reproductive partitioning, estimates of effective population size based on worker and gyne samples are not interchangeable.     

Negative density-dependent emigration of males in an increasing red deer population

In species with polygynous mating systems, females are regarded as food-limited, while males are limited by access to mates. When local density increases, forage availability declines, while mate access for males may increase due to an increasingly female-biased sex ratio. Density dependence in emigration rates may consequently differ between sexes. Here, we investigate emigration using mark-recovery data from 468 young red deer Cervus elaphus marked in Snillfjord, Norway over a 20-year period when the population size has increased sixfold. We demonstrate a strong negative density-dependent emigration rate in males, while female emigration rates were lower and independent of density. Emigrating males leaving the natal range settled in areas with lower density than expected by chance. Dispersing males moved 42 per cent longer at high density in 1997 (37 km) than at low density in 1977 (26 km), possibly caused by increasing saturation of deer in areas surrounding the marking sites. Our study highlights that pattern of density dependence in dispersal rates may differ markedly between sexes in highly polygynous species. Contrasting patterns reported in small-scale studies are suggestive that spatial scale of density variation may affect the pattern of temporal density dependence in emigration rates and distances.     

Levels of clonal mixing in the black bean aphid Aphis fabae, a facultative ant mutualist

Aphids are a worldwide pest and an important model in ecology and evolution. Little is known, however, about the genetic structure of their colonies at a microgeographic level. For example, it remains largely unknown whether most species form monoclonal or polyclonal colonies. Here, we present the first detailed study on levels of clonal mixing in a nonsocial facultative ant mutualist, the black bean aphid Aphis fabae. In contrast to the earlier suggestion that colonies of this species are generally monoclonal, we found that across two subspecies of the black bean aphid, A. fabae cirsiiacanthoidis and A. fabae fabae, 32% and 67% of the aphid colonies were in fact polyclonal, consisting of a mix of up to four different clones, which resulted in an overall average relatedness within colonies of 0.90 and 0.79 in the two subspecies. Data further show that the average relatedness in A. f. cirsiiacanthoidis remained relatively constant throughout the season, which means that clonal erosion due to clonal selection more or less balanced with the influx of new clones from elsewhere. Nevertheless, relatedness tended to decrease over the lifetime of a given colony, implying that clonal mixing primarily resulted from the joining of pre‐existing colonies as opposed to via simultaneous host colonisation by several foundresses. Widespread clonal mixing is argued to affect the ecology and evolution of the aphids in various important ways, for example with respect to the costs and benefits of group living, the evolution of dispersal and the interaction with predators as well as with the ant mutualists.     

Male parentage does not vary with colony kin structure in a multiple-queen ant

Kin selection theory predicts that, in social Hymenoptera, the parentage of males should be determined by within-colony relatedness. We present a model showing that, when sex ratios are split (bimodal) as a function of colony kin structure, the predictions of kin selection theory regarding the occurrence of worker reproduction and policing (prevention of worker reproduction) require modification. To test the predictions of kin selection theory and our model, we estimated using microsatellites the frequency of worker-produced male eggs and adults in the facultatively polygynous (multiple-queen) ant Leptothorax acervorum. Analysis of 210 male eggs and 328 adult males from 13 monogynous (single-queen) and nine polygynous colonies demonstrated that the frequency of worker-produced males was low (2.3-4.6% of all males) and did not differ significantly between colony classes or between eggs and adults. This suggested workers' self-restraint as the cause of infrequent worker reproduction in both colony classes. Such an outcome is not predicted either by comparing relatedness values or by our model. Therefore, it appears that factors other than colony kin structure and sex ratio effects determine the pattern of male parentage in the study population. A likely factor is a colony-level cost of worker reproduction.     

Effect of habitat saturation on the number and turnover of queens in the polygynous ant,Myrmica sulcinodis

In polygynous social insects more than one queen reproduces in a colony. In such populations ecological factors affecting survival and reproduction of queens are likely to be of prime importance for social organization. In particular, habitat saturation leading to severe limitations in the availability of nest sites has been suggested to promote high queen number. In this study we examine the social and genetic structure of colonies in the polygynous ant Myrmica sulcinodis. We investigated a single breeding population in two adjacent habitats which differed markedly in the availability of nest sites. In the main habitat M. sulcinodis occupied almost all suitable nest sites, whereas in the other (marginal) habitat most sites were unoccupied by ants, due to a recent fire. In support of the habitat saturation hypothesis, the number of queens per colony which could explain the estimated relatedness among workers was almost five times higher for the main habitat than for the marginal habitat. This is the first demonstration that the kin structure of a social insect population is plastic and responds adaptively to short-term changes in ecological constraints such as nest site availability. Based on combined genetic and demographic data we discuss queen reproductive strategies and suggest that a special class of queen ‘floaters’ only stays ephemerally in the colonies, thus causing a substantial turnover of reproducing queens across years.     

Sources of stochasticity in models of sex allocation in spatially structured populations

There are many ways to include stochastic effects in models of sex allocation evolution. These include variability in the number of mating partners and fecundity in a rich literature that goes back 20 years. The effects of variance in the fecundity and number of mating partners have typically been considered separately from the stochastic effects of mortality. However, I show that these processes produce mathematically equivalent models with subtly different biological details. These scenarios differ in the way that information becomes available to individuals because the parents often have information on mating partners while they are making sex allocation decisions, but must make these decisions before brood mortality takes place. This makes it possible to test which mechanism, stochastic mortality or variation in mating partners, is responsible for observed sex ratios. Alternatively, asymmetric variance between sexual functions can cause skewed sex allocation, even in the absence of local mate competition. This allows the evolution of either female- or male-biased sex ratios depending on which sexual function is more variable.     

Seed sex ratio in dioecious plants depends on relative dispersal of pollen and seeds: an example using a chessboard simulation model

Two principles are important for the optimal sex ratio strategy of plants. (1) Sib mating. Because seed dispersal is restricted, sib mating may occur which selects for a female bias in the seed sex ratio. (2) Local resource competition (LRC). If a plant produces pollen its nuclear genes are dispersed in two steps: first through the pollen and then, if the pollen is successful in fertilizing an ovule on another plant, through the seed. If the plant produces an ovule, its genes are dispersed only through the seed. By making pollen instead of ovules the offspring of a single plant is then spread out over a wider area. This reduces the chance that genetically related individuals are close together and need to compete for the same resource. The effect is the strongest if pollen is dispersed over a much wider area than seeds. Less LRC for paternally vs. maternally derived offspring selects for a male bias in sex allocation. We study the above‐mentioned opposite effects in dioecious plants (with separate male and female individuals), with maternal control over the sex ratio (fraction males) in the seeds. In a two‐dimensional spatial model female‐biased sex ratios are found when both pollen and seed dispersal are severely restricted. If pollen disperses over a wider area than seeds, which is probably the common situation in plants, the seed sex ratio becomes male‐biased. If pollen and seeds are both dispersed over a wide area, the sex ratio approaches 0.5. Our results do not change if the offspring of brother–sister matings are less fit because of inbreeding depression.