Competition between relatives and the evolution of dispersal in a parasitoid wasp

Evolutionary theory predicts that levels of dispersal vary in response to the extent of local competition for resources and the relatedness between potential competitors. Here, we test these predictions by making use of a female dispersal dimorphism in the parasitoid wasp Melittobia australica. We show that there are two distinct female morphs, which differ in morphology, pattern of egg production, and dispersal behaviour. As predicted by theory, we found that greater competition for resources resulted in increased production of dispersing females. In contrast, we did not find support for the prediction that high relatedness between competitors increases the production of dispersing females in Melittobia. Finally, we exploit the close links between the evolutionary processes leading to selection for dispersal and for biased sex ratios to examine whether the pattern of dispersal can help distinguish between competing hypotheses for the lack of sex ratio adjustment in Melittobia.     

Sex ratio polymorphism: The impact of mutation and drift on evolution

This paper addresses the question, which sex ratio will evolve in a population that is subject to mutation and drift. The problem is analyzed using a simulation model as well as analytical methods. A detailed simulation model for the evolution of a population's allele distribution shows that for the sex ratio game a wide spectrum of different population states may evolve from on the one hand a monomorphic state with one predominant allele and with all other alleles suppressed by the forces of selection, to on the other hand a polymorphism determined by recurrent mutations. Which of these states will evolve depends on the population size, the mating system and the rate of mutations. For the sex ratio game the evolutionary stable strategy (ESS), as defined by evolutionary game theory, can only predict the population sex ratio but not the underlying stable population state. A comparison of different approaches to the problem shows that false predictions of the stable population states might result from two simplifying assumptions that are fairly common in evolutionary biology: a) it is assumed that mutations are rare events and there is never more than one mutant gene present in a population at any one time; b) a deterministic relationship is assumed between the fitness assigned to an individual's strategy and the individual's contribution to the gene pool of future generations.     

The Comparative Biology of Genetic Variation for Conditional Sex Ratio Behavior in a Parasitic Wasp, Nasonia Vitripennis

Using genetic markers, we tracked the sex ratio behavior of individual females of the parasitic wasp, Nasonia vitripennis, in foundress groups of size 1, 2, 4, 8 and 16. Comparison of 12 isofemale strains extracted from a natural population reveals significant between-strain heterogeneity of sex ratios produced in all sizes of foundress group. Under simple assumptions about population structure, this heterogeneity results in heterogeneity of fitnesses. The strains differ in their conditional sex ratio behavior (the sex ratio response of a female to foundress groups of different sizes). Females of some strains produce more males as foundress group size increases (up to size eight). Females of another strain produce more males when not alone but do not respond differentially to group size otherwise. Females of two other strains show no conditional sex ratio behavior. Females of only two strains behave differently in foundress groups of size 8 and 16. Correlation and regression analyses indicate that the strains differ significantly in their fit to the predictions of an evolutionarily stable strategy (ESS) model of conditional sex ratio behavior. Such heterogeneity contradicts the notion that females of this species possess conditional sex ratio behavior that is optimal in the ESS sense. The results imply that this ESS model is useful but not sufficient for understanding the causal basis of the evolution of this behavior in this species. This is the first report on the sex ratio behavior of individual females in multiple foundress groups in any species of parasitic wasp. Data of this type (and not foundress group or ``patch'''' sex ratios) are essential for testing evolutionary models that predict the sex ratio behaviors of individuals. We suggest that a test for an ESS model include the answers to two important questions: 1) is the model quantitatively accurate? and 2) is there reasonable evidence to indicate that natural selection has caused individuals to manifest the ESS behavior?     

The dynamical attainability of ESS in evolutionary games

In this paper, the attainability of ESS of the evolutionary game among n players under the frequency-independent selection is studied by means of a mathematical model describing the dynamical development and a concept of stability (strongly determined stability). It is assumed that natural selection and small mutations cause the phenotype to change gradually in the direction of fitness increasing. It is shown that (1) the ESS solution is not always evolutionarily attainable in the evolutionary dynamics, (2) in the game where the interaction between two species is completely competitive, the Nash solution is always attainable, and (3) one of two species may attain the state of minimum fitness as a result of evolution. The attainability of ESS is also examined in two game models on the sex ratio of wasps and aphids in light of our criterion of the attainability of ESS.     

Evolutionarily stable sex ratios and sex allocations

The paternal fitness of a sexual individual is equated with the fitness of those eggs of its potential mates which it is able to fertilize. This property enables the total sexual fitness of individuals to be expressed in terms of female gamete contributions in separate equations for a cosex (an individual in a population composed of a single sexual class which combines male and female functions) and for parents in a dioecious population. The general equations are used in phenotypic models of selection which examine conditions maximizing the fitness advantage of one phenotype over another with a different sex ratio or allocation. As an example, it is shown that finite population size confers full stability on the sexual allocations in a cosexual population and on the sex ratio in a dioecious population.The use of fitness advantages provides the outcome of selection for all frequencies of contrasted phenotypes. It is therefore possible to redefine an ESS to allow for persistent variability in a population. A phenotype is an ESS in a population if, from any initial frequency, it is protected from loss by its fitness advantage. The conditions for a rare mutant to spread invariably coincide with those for its fixation only if an individual of any phenotype affects the fitness of other individuals of all phenotypes in identical ways.     

Evolutionarily stable strategies in food selection models with fitness sets

Most current models for optimal food selection apply to ecological and behavioural optimization. In this paper optimal food selection theory is extended to apply to evolutionary optimization. A general evolutionary model for optimal food selection must incorporate the concept of fitness sets--or that variables, changing as a result of natural selection in evolutionary time, cannot, in general, vary independently of each other. A "Charnov type" optimal food selection model with a fitness set is investigated, and evolutionarily stable strategy (ESS) solutions of the evolutionary variables (i.e., the efficiencies of using available food types) are found. From this analysis it follows that the relative frequency of various food types in the environment may, under specified conditions, influence the evolutionarily optimal diet. Secondly, the analysis demonstrates that a food type not in the optimal diet may, in evolutionary time, be added to this by becoming more abundant. Thirdly, it follows from the analysis that the ecological result of MacArthur and Pianka, that food types are worth eating even if there is competition for them, is not generally applicable when referring to an evolutionary time scale. Finally, it is pointed out that for the diet to be an ESS, it is necessary that the consumer's density is stable and that the consumer's population dynamics are subjected to some density-dependent factor.     

The relationship between host selection behaviour and offspring fitness in a koinobiont parasitoid

1. When host quality varies, optimal foraging theory assumes that parasitic wasps select hosts in a manner that increases their individual fitness. In koinobiont parasitoids, where the hosts continue developing for a certain period of time after parasitisation, host selection may not reflect current host quality but may be based on an assessment of future growth rates and resources available for the developing larvae. 2. When presented with hosts of uniform quality, the koinobiont parasitoid Leptomastix dactylopii exhibits a characteristic host‐selection behaviour: some hosts are accepted for oviposition on first encounter, while others are rejected several times before an egg is laid in them, a behaviour that is commonly associated with a changing host acceptance threshold during the course of a foraging bout. 3. The fitness of the offspring that emerged from hosts accepted immediately upon encounter was compared with the fitness of offspring emerged from hosts rejected several times before being accepted for oviposition. 4. The pattern of host acceptance and rejection was not related to any of the measured fitness parameters of the offspring emerging from these hosts (development time, size at emergence, sex ratio at emergence, and female offspring egg load). 5. While complex post facto adaptive explanations can be devised to explain the nature of such a time and energy consuming host selection process, it is suggested that physiological constraints on egg production or oviposition may provide an alternative, purely mechanistic, explanation for the results obtained.     

High brood patch temperature of less colourful,less pheomelanic female Barn Swallows Hirundo rustica

In birds, even a minor difference in egg temperature (1–1.5 °C) has been shown to affect the fitness of offspring by changing hatching success, incubation period and nestling quality. Female, but not male, passerines develop brood patches. Thus if there are traits, such as plumage ornamentation, that indicate optimal egg temperature, males should pair with females that exhibit those traits. However, no study has yet investigated the relationship between female brood patch temperature, which would directly affect egg temperature, and female plumage ornamentation. In this study, we examined the surface temperature of female brood patches during nocturnal incubation and examined its relationship with female plumage ornaments in Asian Barn Swallows Hirundo rustica gutturalis. After controlling for ambient air temperature, brood patch temperature was negatively associated with colour saturation of the female throat patch. No other female ornaments, such as tail‐length, white tail spots or throat patch size, predicted brood patch temperature. When oral (mouth) temperature was statistically controlled, females with less colourful throats and longer tails showed higher brood patch temperature, indicating that these females had hotter brood patches in relation to the temperature of other body parts. Furthermore, we found a negative relationship between pheomelanin pigmentation and brood patch temperature after controlling for ambient air temperature or oral temperature. To our knowledge, this is the first study to show that female ornaments can predict the absolute/relative thermal investment in brood patches. This relationship, together with other aspects of female quality, may affect male mate preference and female ornamentation.     

The evolution of parental care in the context of sexual selection: a critical reassessment of parental investment theory

Males and females are often defined by differences in their energetic investment in gametes. In most sexual species, females produce few large ova, whereas males produce many tiny sperm. This difference in initial parental investment is presumed to exert a fundamental influence on sex differences in mating and parental behavior, resulting in a taxonomic bias toward parental care in females and away from parental care in males. In this article, we reexamine the logic of this argument as well as the evolutionarily stable strategy (ESS) theory often used to substantiate it. We show that the classic ESS model, which contrasts parental care with offspring desertion, violates the necessary relationship between mean male and female fitness. When the constraint of equal male and female mean fitness is correctly incorporated into the ESS model, its results are congruent with those of evolutionary genetic theory for the evolution of genes with direct and indirect effects. Male parental care evolves whenever half the magnitude of the indirect effect of paternal care on offspring viability exceeds the direct effect of additional mating success gained by desertion. When the converse is true, desertion invades and spreads. In the absence of a genetic correlation between the sexes, the evolution of paternal care is independent of maternal care. Theories based on sex differences in gametic investment make no such specific predictions. We discuss whether inferences about the evolution of sex differences in parental care can hold if the ESS theory on which they are based contains internal contradictions.     

Does the differential cost of sons and daughters lead to sex ratio adjustment in great frigatebirds Fregataminor?

Sex allocation theory predicts that if benefits of producing sons and daughters differ and outweigh the costs of sex ratio adjustment, parents should produce more of the offspring that provide them with greater fitness. Potential benefits may be more likely to outweigh costs where sexual size dimorphism and, in birds, single‐egg clutches exist. Great frigatebirds Fregataminor are seabirds in which females are larger than males and clutch size is one egg. In our study population, sexual size dimorphism develops primarily during the period of complete juvenile dependence on parental care, consistent with a higher cost of producing daughters than sons. Over the course of the 1998 breeding season there was a shift from early season prevalence of daughters to late‐season prevalence of sons. Variation in food availability at time of egg laying, as indexed by sea surface temperature (SST), was a strong predictor of offspring sex in 1998. In contrast, SST in 2003 was not a predictor of offspring sex, nor was there a seasonal shift in the hatching sex ratio, despite a seasonal shift in SST. Besides food availability, we tested two additional factors in 2003 that could explain sex ratio adjustment in relation to the cost of reproduction. Offspring sex in 2003 was not related to natural or experimentally induced variation in maternal body condition; pre‐laying food supplements raised the body condition of females at the time of egg laying but did not affect offspring sex or egg mass. In addition, offspring sex was not predicted by the length of maternal telomere restriction fragments (TRFs), an index of age and possibly of reproductive experience. Broad confidence intervals on effect size suggest that undetected effects of maternal condition on offspring sex ratio could easily exist, but confidence intervals were narrower on the non‐significant effects of SST and TRF length on offspring sex ratio. The cause of different seasonal patterns of hatching sex ratio and different SST effects in 1998 and 2003 is unclear.     

Novel evolutionary pathways of sex‐determining mechanisms

Evolutionary transitions between sex‐determining mechanisms (SDMs) are an enigma. Among vertebrates, individual sex (male or female) is primarily determined by either genes (genotypic sex determination, GSD) or embryonic incubation temperature (temperature‐dependent sex determination, TSD), and these mechanisms have undergone repeated evolutionary transitions. Despite this evolutionary lability, transitions from GSD (i.e. from male heterogamety, XX/XY, or female heterogamety, ZZ/ZW) to TSD are an evolutionary conundrum, as they appear to require crossing a fitness valley arising from the production of genotypes with reduced viability owing to being homogametic for degenerated sex chromosomes (YY or WW individuals). Moreover, it is unclear whether alternative (e.g. mixed) forms of sex determination can persist across evolutionary time. It has previously been suggested that transitions would be easy if temperature‐dependent sex reversal (e.g. XX male or XY female) was asymmetrical, occurring only in the homogametic sex. However, only recently has a mechanistic model of sex determination emerged that may allow such asymmetrical sex reversal. We demonstrate that selection for TSD in a realistic sex‐determining system can readily drive evolutionary transitions from GSD to TSD that do not require the production of YY or WW individuals. In XX/XY systems, sex reversal (female to male) occurs in a portion of the XX individuals only, leading to the loss of the Y allele (or chromosome) from the population as XX individuals mate with each other. The outcome is a population of XX individuals whose sex is determined by incubation temperature (TSD). Moreover, our model reveals a novel evolutionarily stable state representing a mixed‐mechanism system that has not been revealed by previous approaches. This study solves two long‐standing puzzles of the evolution of sex‐determining mechanisms by illuminating the evolutionary pathways and endpoints.     

Phenotypic consequences of incubation environment in the African elapid genus Aspidelaps

Eggs and embryos of the African elapid genus Aspidelaps were tested for phenotypic plasticity in response to incubation temperature and hygration. Fifty-two fertile eggs, representing both A. lubricus and A. scutatus, were utilized over two successive breeding seasons. Interspecific difference in hatchling snout-vent length (SVL) was significant, but the two species were equivalent in initial egg mass and hatchling mass. Hatchling mass was unaffected by temperature and incubation substrate moisture, but was positively correlated to initial egg mass. In A. lubricus, SVL was influenced by an incubation temperature-substrate moisture interaction. In A. scutatus, SVL was unaffected by the experimental variables. The secondary sex ratio among hatchlings was significantly female skewed under mesic incubation conditions, and male skewed under xeric conditions. One explanation for the biased sex ratios is differential mortality at wet and dry conditions. The results indicate the two species of Aspidelaps are uniform with regard to female investment in egg and hatchling biomass, yet they partition resources differently during embryogenesis to yield morphologically distinct neonates. © 1996 Wiley-Liss, Inc.     

When should a female avoid adding eggs to the clutch of another female? A simultaneous oviposition and sex allocation game

Summary Avoidance of double oviposition (ADO) is the strategy not to oviposit on food patches where another female has oviposited before. If two females oviposit on the same patch, competitive and mating interactions within and between broods may lead to both a clutch size game and a sex allocation game between the two visitors. Though the two games interact, they are usually considered separately. Here, the ESS conditions for ADO are investigated in an analysis that combines the two games into one. The analysis strengthens the notion that it is really ADO that needs to be explained, because role-dependent net pay-off from an additional egg is most likely to favour double oviposition (DO). To a first female, the net payoff includes the effect on the eggs already present, whereas to a second female only the egg's gross pay-off matters. ADO is the evolutionary stable strategy (ESS) if there are enough patches still without eggs and either (1) the fitness of an additional egg is so low that the first female would not lay it even in the absence of detrimental effects on earlier offspring, so neither would a second female, or (2) differences in either the survival probability of the offspring or their reproductive success are sufficient to counterbalance the differential interest in the eggs already present. The first condition requires that eggs are relatively large, because then the decrease in pay-off between two successive eggs can be large. The second condition may be met when there is a time interval between ovipositions of subsequent females. The resulting developmental lag of the second clutch will (1) diminish its ability to compete for food and (2) lower its reproductive success when there is local mate competition and sons are too late to mate with daughters of the first female. If sons of first and second females compete on equal terms, however, ADO is unlikely. Male migration between patches reduces the influence of sex allocation strategies on clutch size decisions; the same holds for small clutch sizes. To illustrate the importance of considering sex allocation and clutch size decisions in an integrated way, oviposition strategies of plant-inhabiting predatory mites (Acari: Phytoseiidae) are discussed.     

The evolution of different maternal investment strategies in two closely related desert vertebrates

We compared egg size phenotypes and tested several predictions from the optimal egg size (OES) and bet‐hedging theories in two North American desert‐dwelling sister tortoise taxa, Gopherus agassizii and G. morafkai, that inhabit different climate spaces: relatively unpredictable and more predictable climate spaces, respectively. Observed patterns in both species differed from the predictions of OES in several ways. Mean egg size increased with maternal body size in both species. Mean egg size was inversely related to clutch order in G. agassizii, a strategy more consistent with the within‐generation hypothesis arising out of bet‐hedging theory or a constraint in egg investment due to resource availability, and contrary to theories of density dependence, which posit that increasing hatchling competition from later season clutches should drive selection for larger eggs. We provide empirical evidence that one species, G. agassizii, employs a bet‐hedging strategy that is a combination of two different bet‐hedging hypotheses. Additionally, we found some evidence for G. morafkai employing a conservative bet‐hedging strategy. (e.g., lack of intra‐ and interclutch variation in egg size relative to body size). Our novel adaptive hypothesis suggests the possibility that natural selection favors smaller offspring in late‐season clutches because they experience a more benign environment or less energetically challenging environmental conditions (i.e., winter) than early clutch progeny, that emerge under harsher and more energetically challenging environmental conditions (i.e., summer). We also discuss alternative hypotheses of sexually antagonistic selection, which arise from the trade‐offs of son versus daughter production that might have different optima depending on clutch order and variation in temperature‐dependent sex determination (TSD) among clutches. Resolution of these hypotheses will require long‐term data on fitness of sons versus daughters as a function of incubation environment, data as yet unavailable for any species with TSD.     

Factors influencing brood sex ratios in polyembryonic Hymenoptera

Copidosoma sp. is a polyembryonic encyrtid wasp which parasitizes isolated hosts. Most broods of this wasp are unisexual, but some contain both sexes and the secondary sex ratio of these is usually highly female biased. The overall population secondary sex ratio is female biased. Walter and Clarke (1992) argue that because the majority of individuals must mate outside the natal patch, the bias in the population secondary sex ratio contradicts predictions made by Hamilton's (1967) theory of local mate competition (LMC). We suggest that the primary sex ratio is unbiased and that Walter and Clarke's results do not cast doubt on LMC. Instead these results imply that ovipositing females make a combined clutch size and sex ratio decision influencing whether individuals developing from a particular brood will outbreed or largely inbreed; for each case the predictions of LMC theory are not violated. If this interpretation is correct, what is of interest is the basis on which this decision is made rather than the population secondary sex ratio. We show that host encounter rate influences the proportions of mixed and single sex broods laid by Copidosoma floridanum, a related polyembryonic parasitoid. Among single-sex broods the primary sex ratio is female biased, but our results are in agreement with LMC theory since offspring developing from these broods will probably mate with siblings from adjacent hosts. We consider the egg load of females to be of major influence on oviposition behaviour, and that the mating structure of parasitoid offspring, potentially differential costs of male and female broods and the natural distributions of hosts both at oviposition and eclosion, require further study.     

Evolutionary dynamics of the Trivers–Willard effect: A nonparametric approach

The Trivers–Willard hypothesis (TWH) states that parents in good condition tend to bias their offspring sex ratio toward the sex with a higher variation in reproductive value, whereas parents in bad condition favor the opposite sex. Although the TWH has been generalized to predict various Trivers–Willard effects (TWE) depending on the life cycle of a species, existing work does not sufficiently acknowledge that sex‐specific reproductive values depend on the relative abundances of males and females in the population. If parents adjust their offspring sex ratio according to the TWE, offspring reproductive values will also change. This should affect the long‐term evolutionary dynamics and might lead to considerable deviations from the original predictions.In this paper, I model the full evolutionary dynamics of the TWE, using a published two‐sex integral projection model for the Columbian ground squirrel (Urocitellus columbianus). Offspring sex ratio is treated as a nonparametric continuous function of maternal condition. Evolutionary change is treated as the successive invasion of mutant strategies. The simulation is performed with varying starting conditions until an evolutionarily stable strategy (ESS) is reached.The results show that the magnitude of the evolving TWE can be far greater than previously predicted. Furthermore, evolutionary dynamics show considerable nonlinearities before settling at an ESS. The nonlinear effects depend on the starting conditions and indicate that evolutionary change is fastest when starting at an extremely biased sex ratio and that evolutionary change is weaker for parents of high condition. The results show neither a tendency to maximize average population fitness nor to minimize the deviation between offspring sex ratio and offspring reproductive value ratio.The study highlights the importance of dynamic feedback in models of natural selection and provides a new methodological framework for analyzing the evolution of continuous strategies in structured populations.     

Egg incubation temperature differently affects female and male hatching dynamics and larval fitness in a leafhopper

Temperature effects on ectotherms are widely studied particularly in insects. However, the life-history effects of temperature experienced during a window of embryonic development, that is egg stage, have rarely been considered. We simulated fluctuating temperatures and examined how this affects the operational sex ratio (OSR) of hatching as well as nymph and adult fitness in a leafhopper, Scaphoideus titanus. Specifically, after a warm or cold incubation we compared males and females hatching dynamics with their consequences on the sex ratio in the course of time, body size, weight, and developmental rate of the two populations, all reared on the same posthatching temperature. Males and females eggs respond differently, with females more sensitive to variation in incubation temperature. The different responses of both sexes have consequences on the sex ratio dynamic of hatchings with a weaker protandry after warm incubation. Temperatures experienced by eggs have more complex consequences on posthatching development. Later nymphal instars that hatched from eggs exposed to warm temperature were larger and bigger but developmental rate of the two populations was not affected. Our study demonstrates how incubation temperature could affect operational sex ratio and posthatching development in an insect and how this may be critical for population growth.     

Genetic variation in sex allocation in a parasitic wasp: variation in sex pattern within sequences of oviposition

In order to maximize their fitness under Local Mate Competition (LMC), arrhenotokous female wasps have to produce a precise sex ratio when encountering hosts. Recent progress in the theory of hymenopterous parasitoid reproduction suggest that they manage to do it by laying male and female eggs in a particular order and that such reproductive strategies are adaptive. Therefore, the determinism of such sequential patterns would be regulated by genetic control on which natural selection could act. To test this hypothesis, sequences of oviposition were recorded in a set ofTrichogramma brassicae Bezdenko (Hymenoptera; Trichogrammatidae) females and in their daughters by providing themEphestia kuehniella Zeller (Lepidoptera; Pyralidae) eggs. In order to describe accurately sex pattern within these oviposition sequences, I present a joined non-parametric and multivariate statistical method. It is shown thatT. brassicae females do not produce male and female eggs in random sequences. Moreover, the way they organize the sequence of the sexes in their progeny seems to be under a strong genetic control. The evolutionary consequences of such results are discussed.     

The Influence of Incubation Conditions and Sex on Growth and Dispersal in Hatchling Lizards

Dispersal is a critical process that has profound influence on ecological and evolutionary processes. Many proximate factors influence natal dispersal, but it is currently unclear whether the conditions experienced during incubation play an important role. We manipulated incubation temperature and used mark–recapture of released hatchlings to test this hypothesis. We tested this hypothesis on the prairie lizard (Sceloporus consobrinus) using two experimental islands in a local reservoir. Incubation conditions influenced some aspects of hatchling morphology, but had little influence on the probability of dispersal. As generally predicted for a polygynous species, males were more likely to disperse than females; however, the growth rate of dispersing vs. resident individuals varied depending on sex. Dispersive male lizards did not grow faster than resident males, whereas female dispersers grew significantly slower than resident females. Although our study was not specifically designed to test for differential costs of dispersal for males and females, this pattern is consistent with recent research demonstrating sex‐specific fitness costs of dispersal.     

Evolution of sex ratios in social hymenoptera: Consequences of finite brood size

Evolutionarily stable sex ratios are determined for social hymenoptera under local mate competition (LMC) and when the brood size is finite. LMC is modelled by the parameterd. Of the reproductive progeny from a single foundress nest, a fractiond disperses (outbreeding), while (l-d) mate amongst themselves (sibmating). When the brood size is finite,d is taken to be the probability of an offspring dispersing, and similarly,r, the proportion of male offspring, the probability of a haploid egg being laid. Under the joint influence of these two stochastic processes, there is a nonzero probability that some females remain unmated in the nest. As a result, the optimal proportion of males (corresponding to the evolutionarily stable strategy, ESS) is higher than that obtained when the brood size is infinite. When the queen controls the sex ratio, the ESS becomes more female biased under increased inbreeding (lowerd). However, the ESS under worker control shows an unexpected pattern, including anincrease in the proportion ofmales withincreased inbreeding. This effect is traced to the complex interaction between inbreeding and local mate competition.