Sex Ratio Theory Research Articles

Queen recruitment and split sex ratios in polygynous colonies of the ant Formica exsecta

Sex ratios in social insects have become a general model for tests of inclusive fitness theory, sex ratio theory and parent–offspring conflict. In populations of Formica exsecta with multiple queens per colony, sex ratios vary greatly among colonies and the dry‐weight sex ratio is extremely male‐biased, with 89% of the colonies producing males but no gynes (reproductive females). Here we test the queen‐replenishment hypothesis, which was proposed to explain sex ratio specialization in this and other highly polygynous ants (i.e. those with many queens per nest). This hypothesis proposes that, in such ants, colonies produce gynes to recruit them back into the colony when the number of resident queens falls below a given threshold limiting colony productivity or survival. We tested predictions of the queen‐replenishment hypothesis by following F. exsecta colonies across two breeding seasons and relating the change in effective queen number with changes in sex ratio, colony size and brood production. As predicted by the queen‐replenishment hypothesis, we found that colonies that specialized in producing females increased their effective queen number and were significantly more likely to specialize in male production the following year. The switch to male production also coincided with a drop in productivity per queen as predicted. However, adoption of new queens did not result in a significant increase in total colony productivity the following year. We suggest that this is because queen production comes at the expense of worker production and thus queen production leads to resource limitation the following year, buffering the effect of greater queen number on total productivity.

Sex ratio variation in a facultatively polygynous ant with size-dimorphic queens

Sex ratio studies in social Hymenoptera have yielded invaluable tests of kin selection and sex ratio theory. However, relatively few studies exist in facultatively polygynous ant species in which alternative reproductive tactics (independent colony founding versus re-adoption of daughter queens and colony budding) make sex ratio predictions more complex. Generally, a decreased proportional investment in female sexual offspring with increasing degree of polygyny is expected from sex ratio theory. The kin conflict over caste determination hypothesis predicts a larger fraction of females will develop into queens when queen/worker dimorphism is low, and thus it predicts an increased proportional investment in female sexual offspring in microgynous (small queen) colonies. As microgyny and polygyny are correlated in the queen-size-dimorphic ant Leptothorax rugatulus, sex ratio theory and the kin conflict over caste determination hypothesis yield contrasting predictions about its sex ratio patterns. While the former predicts a male bias in the offspring from polygynous, microgynous colonies because relatedness asymmetry is low, the latter hypothesis predicts more new queens due to the lower queen/worker dimorphism that facilitates self-determination of the female larvae. In six populations with different social structure and queen morphology we investigated whether the sex ratio variation in this species accords with the prediction of either hypothesis. At the population level, relative female investment decreased significantly with an increasing degree of polygyny, in accordance with sex ratio theory. At the colony level, sex ratios were highly variable but were correlated neither with polygyny nor queen morphology. Resource level played a significant role in only one population. Furthermore, we found no significant difference in intracolonial relatedness between male- and female-specializing colonies. Thus, individual colony sex ratios do not conform well with current sex ratio theory. The tendency of L. rugatulus microgynes to produce more new queens than macrogynes under laboratory conditions is not reflected in our field data. Consequently, we conclude that microgyny does not constitute an effective selfish strategy of caste disguise in the context of kin conflict over caste determination.

PATTERNS OF SEX RATIO VARIATION IN HOUSE SPARROWS

Abstract PCR amplification of a sex-linked gene was used to assay the sex ratio of nestling House Sparrows (Passer domesticus) from five consecutive breeding seasons. We tested several predictions from sex ratio theory, including that at the population level, sparrows should produce a 1:1 sex ratio. Of 1162 nestlings, 53% were male, which is not significantly different from 50%. We did find a significant skew toward males in two of the five years, and significant heterogeneity in sex ratio among seasons. There was no evidence that brood sex ratios were skewed from a binomial distribution, despite a modest excess of all male broods. We found that male nestlings weighed significantly more (0.5 g) than their female siblings. We tested the possibility that females produce males when conditions are good. Sex ratio was not associated with nest attempt, despite some evidence that conditions varied seasonally. Clutch size was negatively associated with date of first egg, but neither nestling weight nor sex ratio ...

HERITABILITY OF SEX TENDENCY IN A HARPACTICOID COPEPOD, TIGRIOPUS CALIFORNICUS

Systems with genetic variation for the primary sex ratio are important for testing sex-ratio theory and for understanding how this variation is maintained. Evidence is presented for heritable variation of the primary sex ratio in the harpacticoid copepod Tigriopus californicus. Variation in the primary sex ratio among families cannot be accounted for by Mendelian segregation of sex chromosomes. The covariance in sex phenotype between full-sibling clutches and between mothers and offspring suggests that this variation has a polygenic basis. Averaged over four replicates, the full-sibling heritability of sex tendency is 0.13 ± 0.040; and the mother-offspring heritability of sex tendency is 0.31 ± 0.216. Genetic correlations in the sex phenotype across two temperature treatments indicate large genotype-by-temperature interactions. Future experiments need to distinguish between zygotic, parental, or cytoplasmic mechanisms of sex determination in T. californicus.

Increased reproductive effort results in male-biased offspring sex ratio: an experimental study in a species with reversed sexual size dimorphism.

Adaptive sex-ratio theory predicts that parents should overproduce the more beneficial offspring sex. Based on a recent experimental study of lesser black-backed gulls, we tested this hypothesis with the great skua, Catharacta skua, a bird species closely related to gulls but where females are the larger sex. When in poor body condition, the gulls overproduced daughters, the smaller and more viable sex under those circumstances. To discriminate between a mandatory physiological overproduction of female (i.e. non-male) eggs versus the overproduction of the smaller and presumably more viable sex, we conducted an egg-removal experiment with the great skua. Since the males are smaller, larger size and being male are separated. Through egg removal we induced females to increase egg production effort. Eggs were sexed using a DNA-based technique. Manipulated pairs produced a significant male bias at the end of the extended laying sequence, while the sex ratio in the control group did not differ from unity. Our results present an example of facultative sex-ratio manipulation and support the hypothesis that in sexually dimorphic birds parents overproduce the smaller sex under adverse conditions.

Reproductive skew and split sex ratios in social Hymenoptera.

I present a model demonstrating that, in social Hymenoptera, split sex allocation can influence the evolution of reproductive partitioning (skew). In a facultatively polygynous population (with one to several queens per colony), workers vary in their relative relatedness to females (relatedness asymmetry). Split sex-ratio theory predicts that workers in monogynous (single-queen) colonies should concentrate on female production, as their relatedness asymmetry is relatively high, whereas workers in the polygynous colonies should concentrate on male production, as their relatedness asymmetry is relatively low. By contrast, queens in all colonies value males more highly per capita than they value females, because the worker-controlled population sex ratio is too female-biased from the queens' standpoint. Consider a polygynous colony in a facultatively polygynous population of perennial, social Hymenoptera with split sex ratios. A mutant queen achieving reproductive monopoly would gain from increasing her share of offspring but, because the workers would assess her colony as monogynous, would lose from the workers rearing a greater proportion of less-valuable females from the colony's brood. This sets an upper limit on skew. Therefore, in social Hymenoptera, skew evolution is potentially affected by queen-worker conflict over sex allocation.

Resource allocation in the red ant Myrmica ruginodis– an interplay of genetics and ecology

Abstract Worker-queen conflicts over reproductive allocation (colony maintenance vs. reproduction) and sex allocation (females vs. males) were examined in two populations of the facultatively polygynous ant Myrmica ruginodis. Plasticity of social organization in the form of two co-existing social types (microgyna and macrogyna) has a profound effect on reproductive allocation. Workers control sex allocation by biasing sex ratios towards their own interest, but local resource competition (LRC) because of restricted dispersal of microgyna females resulted in male bias in one study population. Colony sex ratios were split and followed the predictions of the split sex ratio theory: single queen colonies with higher relatedness asymmetry (RA) produced more females than multiple queen colonies with lower RA. Single and multiple queen colonies showed similar patterns in most aspects of their reproduction, and reproductive allocation could not be explained by the hypothesis tested. This suggests that reproductive allocation conflict is of minor importance in M. ruginodis.

Sex Ratio Conflict and Worker Production in Eusocial Hymenoptera

The best known of the conflicts occurring in eusocial Hymenoptera is queen-worker conflict over sex ratio. So far, sex ratio theory has mostly focused on optimal investment in the production of male versus female sexuals, neglecting the investment in workers. Increased investment in workers decreases immediate sexual productivity but increases expected future colony productivity. Thus, an important issue is to determine the queen's and workers' optimal investment in each of the three castes (workers, female sexuals, and male sexuals), taking into account a possible trade-off between production of female sexuals and workers (both castes developing from diploid female eggs). Here, we construct a simple and general kin selection model that allows us to calculate the evolutionarily stable investments in the three castes, while varying the identity of the party controlling resource allocation (relative investment in workers, female sexuals, and male sexuals). Our model shows that queens and workers favor the investment in workers that maximizes lifetime colony productivity of sexual males and females, whatever the colony kin structure. However, worker production is predicted to be at this optimum only if one of the two parties has complete control over resource allocation, a situation that is evolutionarily unstable because it strongly selects the other party to manipulate sex allocation in its favor. Queens are selected to force workers to raise all the males by limiting the number of eggs they lay, whereas workers should respond to egg limitation by raising a greater proportion of the female eggs into sexual females rather than workers as a means to attain a more female-biased sex allocation. This tug-of-war between queens and workers leads to a stable equilibrium where sex allocation is between the queen and worker optima and the investment in workers is below both parties' optimum. Our model further shows that, under most conditions, female larvae are in strong conflict with queens and workers over their developmental fate because they value their own reproduction more than that of siblings. With the help of our model, we also investigate how variation in queen number and number of matings per queen affect the level of conflict between queens, workers, and larvae and ultimately the allocation of resource in the three castes. Finally, we make predictions that allow us to test which party is in control of sex allocation and caste determination.

Sex ratio and Wolbachia infection in the ant Formica exsecta.

Sex allocation data in social Hymenoptera provide some of the best tests of kin selection, parent-offspring conflict and sex ratio theories. However, these studies critically depend on controlling for confounding ecological factors and on identifying all parties that potentially manipulate colony sex ratio. It has been suggested that maternally inherited parasites may influence sex allocation in social Hymenoptera. If the parasites can influence sex allocation, infected colonies are predicted to invest more resources in females than non-infected colonies, because the parasites are transmitted through females but not males. Prime candidates for such sex ratio manipulation are Wolbachia, because these cytoplasmically transmitted bacteria have been shown to affect the sex ratio of host arthropods by cytoplasmic incompatibility, parthenogenesis, male-killing and feminization. In this study, we tested whether Wolbachia infection is associated with colony sex ratio in two populations of the ant Formica exsecta that have been the subject of extensive sex ratio studies. In these populations colonies specialize in the production of one sex or the other. We found that almost all F. exsecta colonies in both populations are infected with Wolbachia. However, in neither population did we find a significant association in the predicted direction between the prevalence of Wolbachia and colony sex ratio. In particular, colonies with a higher proportion of infected workers did not produce more females. Hence, we conclude that Wolbachia does not seem to alter the sex ratio of its hosts as a means to increase transmission rate in these two populations of ants.

Conflict over Sex Allocation Drives Conflict over Reproductive Allocation in Perennial Social Insect Colonies

Queen-worker conflict in the social Hymenoptera has become a cornerstone of sex-ratio theory. Extending that theory to conflict over life-history decisions, however, has proven controversial. Pamilo first proposed that queen-worker conflict over reproductive allocation should be important in perennial, social insect colonies, but Bourke and Chan have questioned the generality of that claim. Here, we reexamine this problem for the simplest case of a monogynous and monandrous hymenopteran society by relaxing assumptions of Pamilo's model. In populations with monomorphic sex ratios, queens and workers agree on allocation to growth versus reproduction. However, variation in sex allocation across colonies can induce queen-worker conflict over reproductive allocation; the former is a necessary condition for the latter. We explore how conflict over reproductive allocation depends on the population-wide sex ratio, the survivorship probabilities for existing colonies, and the likelihood of establishing new colonies. We then test our theory for two ant species, each with two years of data. We find considerable support for our contention of queen-worker conflict over reproductive allocation and suggest how future studies should be structured to explore this conflict further.

A polymorphic effect of sexually differential production costs when one parent controls the sex ratio.

R. A. Fisher's sex ratio theory predicts that if sons and daughters cost fixed amounts of resources to raise and parents have fixed amounts to invest, then the numerical sex ratio of a panmictic population will evolve to be inversely proportional to relative cost. However, the theory assumes control by both parents. We show that allowing one parent to control the sex ratio biases it further from parity than Fisher's theory predicts. Quantitatively, the additional bias towards the cheaper sex depends only very weakly on which sex is in control. Qualitatively, however, the effect is very strong: a monomorphic, mixed-brood strategy evolves only if the more expensive sex is in control. If the controlling sex is cheaper to raise, then the sex ratio is instead achieved through a polymorphism of single-sex broods. Such polymorphisms are seldom observed in nature, generating the prediction that wherever the sexes are not equally costly, sex ratio is usually either under biparental control or under uniparental control by the more expensive sex. However, such polymorphisms do occur, and some of them may be explained by our model.

Colony structure of a slavemaking ant. I. Intracolony relatedness, worker reproduction, and polydomy.

Colony and population structure of the obligate slavemaker ant Protomognathus americanus was analyzed via four nuclear microsatellite loci and mitochondrial DNA (mtDNA) markers. Colonies of P. americanus usually contain a single queen, and here we show that she is singly inseminated. Nestmate workers are generally full sisters and their relatedness does not deviate from the expected value of 0.75. Even though colonies were strictly monogynous, we were able to infer that colony takeover by related queens was common and queen replacement by unrelated queens was rare. Polydomy is widespread, with neighboring nests having the same genetic composition. Although we found no evidence of population viscosity or inbreeding from nuclear markers, mtDNA markers provided evidence for small-scale genetic structuring. Haplotype structuring and takeover by related queens suggest philopatry of newly mated queens. In this species, workers reproduce in queenright and queenless nests and worker reproduction accounts for more than 70% of all males. Although sex-ratio theory points to slavemaking ants as important systems for studying queen-worker conflict, our results indicate no basis for such conflict in P. americanus, because extensive worker reproduction generates shifts in relatedness values. Rather, the dual effects of independent polydomous nest units and local resource competition among queens produce male-biased allocation ratios in this species.

Sex Ratio Conflict and Worker Production in Eusocial Hymenoptera

The best known of the conflicts occurring in eusocial Hymenoptera is queen‐worker conflict over sex ratio. So far, sex ratio theory has mostly focused on optimal investment in the production of male versus female sexuals, neglecting the investment in workers. Increased investment in workers decreases immediate sexual productivity but increases expected future colony productivity. Thus, an important issue is to determine the queen’s and workers’ optimal investment in each of the three castes (workers, female sexuals, and male sexuals), taking into account a possible trade‐off between production of female sexuals and workers (both castes developing from diploid female eggs). Here, we construct a simple and general kin selection model that allows us to calculate the evolutionarily stable investments in the three castes, while varying the identity of the party controlling resource allocation (relative investment in workers, female sexuals, and male sexuals). Our model shows that queens and workers favor the investment in workers that maximizes lifetime colony productivity of sexual males and females, whatever the colony kin structure. However, worker production is predicted to be at this optimum only if one of the two parties has complete control over resource allocation, a situation that is evolutionarily unstable because it strongly selects the other party to manipulate sex allocation in its favor. Queens are selected to force workers to raise all the males by limiting the number of eggs they lay, whereas workers should respond to egg limitation by raising a greater proportion of the female eggs into sexual females rather than workers as a means to attain a more female‐biased sex allocation. This tug‐of‐war between queens and workers leads to a stable equilibrium where sex allocation is between the queen and worker optima and the investment in workers is below both parties’ optimum. Our model further shows that, under most conditions, female larvae are in strong conflict with queens and workers over their developmental fate because they value their own reproduction more than that of siblings. With the help of our model, we also investigate how variation in queen number and number of matings per queen affect the level of conflict between queens, workers, and larvae and ultimately the allocation of resource in the three castes. Finally, we make predictions that allow us to test which party is in control of sex allocation and caste determination.

REPRODUCTIVE SKEW AND SPLIT SEX RATIOS IN SOCIAL HYMENOPTERA

I present a model demonstrating that, in social Hymenoptera, split sex allocation can influence the evolution of reproductive partitioning (skew). In a facultatively polygynous population (with one to several queens per colony), workers vary in their relative relatedness to females (relatedness asymmetry). Split sex-ratio theory predicts that workers in monogynous (single-queen) colonies should concentrate on female production, as their relatedness asymmetry is relatively high, whereas workers in the polygynous colonies should concentrate on male production, as their relatedness asymmetry is relatively low. By contrast, queens in all colonies value males more highly per capita than they value females, because the worker-controlled population sex ratio is too female-biased from the queens' standpoint. Consider a polygynous colony in a facultatively polygynous population of perennial, social Hymenoptera with split sex ratios. A mutant queen achieving reproductive monopoly would gain from increasing her share of offspring but, because the workers would assess her colony as monogynous, would lose from the workers rearing a greater proportion of less-valuable females from the colony's brood. This sets an upper limit on skew. Therefore, in social Hymenoptera, skew evolution is potentially affected by queen-worker conflict over sex allocation.Corresponding Editor: K. Ross

COLONY STRUCTURE OF A SLAVEMAKING ANT. I. INTRACOLONY RELATEDNESS, WORKER REPRODUCTION, AND POLYDOMY

Colony and population structure of the obligate slavemaker ant Protomognathus americanus was analyzed via four nuclear microsatellite loci and mitochondrial DNA (mtDNA) markers. Colonies of P. americanus usually contain a single queen, and here we show that she is singly inseminated. Nestmate workers are generally full sisters and their relatedness does not deviate from the expected value of 0.75. Even though colonies were strictly monogynous, we were able to infer that colony takeover by related queens was common and queen replacement by unrelated queens was rare. Polydomy is widespread, with neighboring nests having the same genetic composition. Although we found no evidence of population viscosity or inbreeding from nuclear markers, mtDNA markers provided evidence for small-scale genetic structuring. Haplotype structuring and takeover by related queens suggest philopatry of newly mated queens. In this species, workers reproduce in queenright and queenless nests and worker reproduction accounts for more than 70% of all males. Although sex-ratio theory points to slavemaking ants as important systems for studying queen-worker conflict, our results indicate no basis for such conflict in P. americanus, because extensive worker reproduction generates shifts in relatedness values. Rather, the dual effects of independent polydomous nest units and local resource competition among queens produce male-biased allocation ratios in this species.

Virgin rotifers

Looking at exceptions to well known rules is one of the best ways of deepening our understanding of evolutionary questions. For example, finding explanations for biased ratios has resulted in a much more complete and satisfying picture of sex-ratio theory. This is why ancient, diverse and completely asexual lineages have attracted attention. They seem to be inconsistent with the general picture of short-lived asexual taxa with close sexual relatives 1 Bell G. The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press, 1982 Google Scholar , which fits, at least in broad terms, with current theory. Although there is little agreement about the relative importance of the many and various proposed advantages of sex 2 Kondrashov A.S. Classification of hypotheses on the advantage of amphimixis. J. Hered. 1993; 84: 372-387 PubMed Google Scholar , 3 West S.A. et al. A pluralist approach to sex and recombination. J. Evol. Biol. 1999; 12: 1003-1012 Crossref Scopus (345) Google Scholar , the common expectation is that the benefits gained by newly arisen asexual lineages, primarily through avoiding the cost of producing males, will be eroded over time. Some combination of the effects of deleterious mutations, or an inability to respond as rapidly as sexual lineages to environmental change, will mean that the asexual lineage is short lived. Hence the pattern of many phylogenetically isolated asexual taxa arising within sexual clades.

Timing of foetal growth spurts can explain sex ratio variation in polygynous mammals

The prediction from sex ratio theory that natural selection on sexually dimorphic mammals should favour an excess of male offspring only when mothers are in good condition, has been tested extensively but with little consistency in results. Although recent studies have shown that environmental variations may cause some of the discrepancy, there have also been reports of contrasting sex ratios under similar environmental settings. Here it is suggested that variation in timing of environmental stress and sex‐specific differences in foetal growth pattern in relation to maternal condition, may explain such seeming contradictions in sex ratio variation of polygynous mammals.

Local Competition, Inbreeding, and the Evolution of Sex-Biased Dispersal.

Using game theory, we developed a kin-selection model to investigate the consequences of local competition and inbreeding depression on the evolution of natal dispersal. Mating systems have the potential to favor strong sex biases in dispersal because sex differences in potential reproductive success affect the balance between local resource competition and local mate competition. No bias is expected when local competition equally affects males and females, as happens in monogamous systems and also in polygynous or promiscuous ones as long as female fitness is limited by extrinsic factors (breeding resources). In contrast, a male-biased dispersal is predicted when local mate competition exceeds local resource competition, as happens under polygyny/promiscuity when female fitness is limited by intrinsic factors (maximal rate of processing resources rather than resources themselves). This bias is reinforced by among-sex interactions: female philopatry enhances breeding opportunities for related males, while male dispersal decreases the chances that related females will inbreed. These results meet empirical patterns in mammals: polygynous/promiscuous species usually display a male-biased dispersal, while both sexes disperse in monogamous species. A parallel is drawn with sex-ratio theory, which also predicts biases toward the sex that suffers less from local competition. Optimal sex ratios and optimal sex-specific dispersal show mutual dependence, which argues for the development of coevolution models.

Spatial dynamics of adaptive sex ratios

According to Fisherian sex allocation theory, parents that can adjust their offspring sex ratio in response to skews in population sex ratio will maximize their fitness over parents lacking this ability. There is good evidence that adaptive sex ratio adjustment occurs in many natural populations, but deviations from theoretical predictions have also been observed. These anomalies may be more apparent than real. When the spatial dimension of sex ratio variation is ignored, then a mismatch between empirical data and theoretical predictions based on panmictic mating is to be expected. We illustrate this with data on human sex ratio variation in 21 preindustrial populations, and with a cellular automaton model built to obey Fisherian sex allocation rules. The results from the model generally match with the data. When information about the ambient sex ratio is limited, then the sex allocation decisions may appear locally maladaptive. In general, the results indicate that Fisher’s sex-ratio theory may have greater explanatory power than previously thought.

Formal Darwinism, the individual–as–maximizing–agent analogy and bet–hedging

The central argument of The origin of species was that mechanical processes (inheritance of features and the differential reproduction they cause) can give rise to the appearance of design. The 'mechanical processes' are now mathematically represented by the dynamic systems of population genetics, and the appearance of design by optimization and game theory in which the individual plays the part of the maximizing agent. Establishing a precise individual-as-maximizing-agent (IMA) analogy for a population-genetics system justifies optimization approaches, and so provides a modern formal representation of the core of Darwinism. It is a hitherto unnoticed implication of recent population-genetics models that, contrary to a decades-long consensus, an IMA analogy can be found in models with stochastic environments (subject to a convexity assumption), in which individuals maximize expected reproductive value. The key is that the total reproductive value of a species must be considered as constant, so therefore reproductive value should always be calculated in relative terms. This result removes a major obstacle from the theoretical challenge to find a unifying framework which establishes the IMA analogy for all of Darwinian biology, including as special cases inclusive fitness, evolutionarily stable strategies, evolutionary life-history theory, age-structured models and sex ratio theory. This would provide a formal, mathematical justification of fruitful and widespread but 'intentional' terms in evolutionary biology, such as 'selfish', 'altruism' and 'conflict'.