The origin of soldiers in the gall-inducing thrips of Australia (Thysanoptera: Phlaeothripidae)

Abstract  For 7 of the 23 described species of Australian gall-inducing thrips, the first individuals of the foundress' brood to eclose are gall-bound soldiers, which are morphologically and behaviourally specialised for defending the fully winged dispersing brood. Additional support is provided for the hypothesis that these self-sacrificing soldiers evolved only once and that there have been two subsequent reversions to a solitary life. Furthermore, this single origin of eusociality took place approximately six million years ago and perhaps four million years after the origin of gall induction in the Acacia thrips. The two losses of the soldier caste may have happened at very different times. One loss may have occurred very soon after the origin of soldiers (approximately 300 000 years later), and the other may have occurred another three million years after that.     

The impact of kleptoparasitic invasions on the evolution of gall-size in social and solitary Australian Acacia thrips

Many species of gall-inducing Acacia thrips are attacked by kleptoparasitic thrips who enter the gall, destroy the occupants, and then use the gall for producing their own offspring. The hypothesis tested here is that pressure exerted by ldeptoparasites （genus Koptothrips） not only provoked the evolution of soldiers in the gall-inducing clade, but have also influenced the evolution of gall size and morphology. Various size dimensions of invaded galls were compared to those of uninvaded galls using data from six gall-inducing species and their kleptoparasites. For the non-social gall-inducing species （K. ellobus and K. nicholsoni） invaded galls showed no significant size differences from galls that had not been invaded. For the four social gall-inducingspecies （K. habrus, K. intermedius, K. waterhousei and K. morrisi） invaded galls were significantly narrower and/or shorter than uninvaded galls. Galls of social species that had not been invaded and contained adult soldiers were significantly larger than galls where soldiers were still at a larval stage, suggesting that gall size is related to gall age in these species. An hypothesis is proposed that links the timing of invasion by kleptoparasites to size of the host gall： induction of a smaller gall by host founders will reduce the period of vulnerability to invasion （before soldiers become adults） for social thrips by allowing foundresses in these smaller galls to begin laying soldierdestined eggs relatively sooner.     

Inbreeding ancestors: the role of sibmating in the social evolution of gall thrips

We used microsatellite data to estimate levels of inbreeding in four species of solitary gall thrips that are in the same clade as the six species with soldier castes. Three of the four species were highly inbred (Fis 0.54-0.68), and the other apparently mated randomly (Fis near zero). These estimates, combined with previous data from species with soldiers, suggest that inbreeding is a pervasive life-history feature of the gall-inducing thrips on Australian Acacia. Mapping of inbreeding estimates onto the phylogeny of the gall inducers showed that the ancestral lineage that gave rise to soldiers was apparently highly inbred, and therefore, inbreeding could have played a role in the origin of sociality within this group. Moreover, there was a trend from high levels of inbreeding at the origin of soldiers to low levels in the most derived species with soldiers, which exhibits the highest levels of reproductive division of labor and soldier altruism. These patterns are consistent with considerations from population genetics, which show that the likelihood of the origin of soldier altruism is higher in inbreeding populations but that, once soldiers have evolved, a reduction in inbreeding levels may facilitate the evolution of enhanced division of labor and reproductive skew.     

Factors influencing the optimum sex ratio in a structured population

W. D. Hamilton (1967, Science 156, 477-488) calculated the optimum sex-ratio strategy for a population subdivided into local mating groups. He made three important assumptions: that the females founding each group responded precisely to the number of them initiating the group; that ail broods within a group matured synchronously; and that males were incapable of dispersing between groups. We have examined the effects of relaxing each of these assumptions and obtained the following results: (1) When broods mature asynchronously the optimum sex ratio is considerably more female biased than the Hamiltonian prediction. (2) Increasing male dispersal always decreases the optimum female bias to the sex ratio, but it is of particular interest that when moderate levels of dispersal are coupled with asynchrony of brood maturation then the optimum strategy is relatively insensitive to changes in foundress number. (3) When females cannot precisely determine the number of other foundresses initiating the group then the optimum strategy is almost exactly the strategy appropriate to a group of average size. These effects can be most easily understood in terms of local parental control (LPC) of the sex ratio. Through LPC a founding female can alter the mating success of her sons by altering the sex ratio of her brood. Asynchrony in the maturation of broods within a group increases the control that a founding female has over the mating success of her sons, whereas male dispersal reduces it. We have shown that the role of LPC and the role of inbreeding, which favors a female-biased sex ratio in haploidiploid species, are independent and that their effects can be combined into a single general formula r = (1-(r2/z2) E(alpha z/alpha r]/(1 + I). The concept of LPC can also be used to interpret two factors which have been proposed to select for the Hamiltonian sex ratios: local mate competition is LPC acting through sons; and sib mating is LPC acting through daughters.     

Seasonal variation in the reproductive strategy of the parasitic wasp Eulophus larvarum (Hymenoptera: Chalcidoidea: Eulophidae)

ABSTRACT. 1. Eulophus larvarum (L.) (Hymenoptera: Eulophidae) is a gregarious parasitoid of lepidopterous larvae feeding on broad-leaved trees. Normally there are two generations a year.
2. Sex ratio in the spring generation of larvae is female biased. The bias is probably due to local mate competition as progeny from one brood emerge from their pupae in close proximity to each other.
3. Sex ratio in the summer generation of larvae is near equality. Local mate competition is absent as individuals from the same brood become separated during the winter.
4. Variation in sex-ratio in the spring generation is consistent with a binomial model. Variation in sex ratio in the summer generation is much greater than expected from a binomial model and there is a large proportion of single-sex broods.
5. Two hypotheses are put forward to explain the summer generation pattern: virgin oviposition, and strong intersexual competition.
6. No differences in clutch size were found between the two generations.     

Egg size and reproductive allocation in eusocial thrips

Reproductive allocation, in terms of fecundity and egg size,has been given little consideration in eusocial societies. Tobegin to address this, absolute and body size–adjustedegg volumes were compared, along with fecundity, between thefoundress and her subfertile soldier offspring in the eusocial,gall-inducing thrips, Kladothrips hamiltoni, Kladothrips waterhousei,and Kladothrips habrus, and a congeneric, Kladothrips morrisi,with fully fecund soldiers. Soldiers produced significantlylarger eggs than the foundress in all species except K. morrisi,where egg volumes did not differ. After accounting for bodysize, soldiers produced significantly smaller eggs than thefoundress in K. morrisi and marginally so in K. waterhousei,but egg sizes did not differ in K. hamiltoni and K. habrus.When egg size and fecundity data are combined, K. morrisi soldiersinvest less in reproduction than the foundress, and in conjunctionwith other life-history features the species can be consideredeusocial. Maximum likelihood analyses reveal relatively lowreproductive allocation skew in the ancestral lineages and highskew in the derived lineages, but the trend is not significantwhen fecundity and egg size are considered separately. Gallsize covaried negatively with soldier-to-foundress relativebody size–adjusted egg size and reproductive allocationand marginally so with fecundity, suggesting that gall sizeis a determinant of egg size and fecundity trade-offs in eusocialthrips and providing the strongest support to date that gallsize has featured in the social evolution of this clade. Thisstudy highlights that data on fecundity alone may be insufficientfor assessing reproductive division of labor.     

Pleometrosis in phyllode-glueing thrips (Thysanoptera: Phlaeothripidae) on Australian Acacia

Pleometrosis, or colony founding by more than one female, is common in various social insects and it engenders opportunities for social cooperation as well as cheating. The life cycles of four species of thrips on Australian Acacia trees were examined to elucidate the extent and nature of colony founding by multiple individuals. Data from colonies of three species of thrips from the genus Dunatothrips Moulton and one species of Lichanothrips Mound were used to infer the prevalence of pleometrosis in each species. The results indicate that Dunatothrips species show high levels of cofounding, with up to 50% of colonies having more than one foundress. By contrast, colonies of Lichanothrips are predominantly established by a female and a male. As in some communal insects, pleometrosis is facultative in Dunatothrips , foundresses show more or less constant per capita reproduction with foundress number, and the selective pressures for pleometrosis may involve predation pressure during founding or survivorship insurance for the brood. In Lichanothrips , male founders are probably engaging in mate guarding, which also occurs in some species of gall-inducing thrips on Acacia . The differences in founding patterns between Dunatothrips and Lichanothrips may be due in part the nature of their domiciles: Dunatothrips engage in extensive construction of a domicile using anal secretions, whereas many Lichanothrips primarily improve a pre-existing partial enclosure. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 75 , 467–474.     

Variation in propensity to defend by reproductive gall morphs in two species of gall-forming thrips

Summary.Six species of Australian phleaothripine gall forming thrips on Acacia have two morphs. One morph, referred to as a soldier, has reduced antennae and wings and greatly enlarged fore femora, which are thought to be adaptations for gall defence. For most species, female soldier morphs have reduced reproductive output relative to dispersing females and these species have been regarded as eusocial. We examine defensive behaviour of soldier morphs using in situ presentation of gall invading kleptoparasites. We show that the gall-morph of Oncothrips tepperi attack kleptoparasites more often (N=87 interactions, n = 11 attacks) than does the gall-morph of Oncothrips morrisi (N = 231, n = 1). This difference in proclivity for defence is coincident with a lower reproductive output by the gall-morph in O. tepperi compared to O. morrisi. Our results also show an almost complete absence of attack behaviour by the gal l-morph of O. morrisi. Lastly, we show that there is no difference in proclivity for defence between soldier and foundress morphs of O. tepperi. These observations taken together call into question the suitability of the term 'soldier' as applied to the gall-morph of the gall-forming thrips of Australia.     

Insemination Capacity and Dispersal in Relation to Sex Allocation Decisions in Goniozus legneri (Hymenoptera: Bethylidae): Why Are There More Males in Larger Broods?

Models considering sex ratio optima under single foundress strict local mate competition predict that female bias will be reduced by stochasticity in sex allocation, developmental mortality of males and limited insemination capacity of males. In all three cases the number of males per brood is expected to increase with brood size. Sex ratio optima may also be less female biased when several mothers contribute offspring to local mating groups or if non‐local mating occurs between members of different broods; again more males are expected in larger broods. In the parasitoid wasp Goniozus legneri (Hymenoptera: Bethylidae), sex allocation has only a small stochastic component, developmental mortality is low and non‐siblings are unlikely to develop in the same brood. However, the number of males per brood increases with the size of the brood (produced by a single mother). We investigated the further possibilities of limited insemination capacity and non‐local mating using a naturalistic experimental protocol. We found that limited insemination capacity is an unlikely general explanation for the increase in number of males with brood size. All males and females dispersed from both mixed and single sex broods. Although most females in mixed sex broods mated prior to dispersal, these data suggest that non‐local mating is possible, for instance via male immigration to broods containing virgin females. This may influence sex ratio optima and account for the trend in male number.     

Evolutionary stable sex ratios with non‐facultative male‐eggs first sex allocation in fig wasps

Sex allocation theory has long generated insights into the nature of natural selection. Classical models have elucidated causal phenomena such as local mate competition and inbreeding on the degree of female bias exhibited by various invertebrates. Typically, these models assume mothers facultatively adjust sex allocation using predictive cues of future offspring mating conditions. Here we relax this assumption by developing a sex allocation model for haplodiploid mothers experiencing local mate competition that lay a fixed number of male eggs first. Female egg number is determined by remaining oviposition sites or remaining eggs of the mother, depending on which is exhausted first. Our model includes parameters for variation in foundress number, patch size, fecundity and offspring mortality that allow us to generate secondary sex ratio predictions based on specific parameterizations for natural populations. Simulations show that: 1) in line with classical models, factors that increase sib‐mating result in mothers laying relatively more female eggs; 2) high offspring mortality leads to relatively more males as fertilization insurance; 3) unlike classical model predictions, sub‐optimal predictions, such as more males than females are possible. In addition, our model provides the first quantitative predictions for the expected number of males and females in a patch where typically only one mother utilizes a given patch. We parameterized the model with data obtained from seven species of southern African fig wasps to predict expected means and variances for numbers of male and female offspring for typical numbers of mothers utilizing a patch. These predictions were compared to secondary sex ratio data from single foundress patches, the most commonly encountered situation for these species. Our predictions matched both the observed number and variance of male and female offspring with a high degree of accuracy suggesting that facultative adjustment is not required to produce evolutionary stable sex ratios.     

Flight muscle breakdown in the soldier caste of the gall-inducing thrips species, Kladothrips intermedius Bagnall

Within the gall-inducing thrips of Australia, genus Kladothrips, is a single origin of a soldier caste. A subsequent radiation has led to at least seven social species, and two species that are likely to have independently lost the soldier caste. Both losses of soldiers are connected to a shift in the insects’ host plant. A third inferred host shift is correlated with life history changes in a species with soldiers, K. intermedius, which might suggest this defensive caste may be in transition. The soldiers of this species have variable wing lengths that overlap with that of the flight-capable dispersers. Our study was designed to assess the possibility that some soldiers in this species retain the ability to disperse by wing. A morphological assessment shows that a proportion of soldiers have body dimensions and wing lengths that fall within the range of dispersers, with males more so than females. However, longer wing length in soldiers (sample of primarily females) did not correspond with a disperser like walking behaviour. Furthermore, histological sections suggest that wing muscles of soldiers are deteriorated or absent, which is similar to what was observed in their foundress mothers. The presence of long wings did not correspond with being flight capable in this caste.     

Increased male sex ratio among brachypterous progeny in Melittobia femorata, a sib-mating parasitoid wasp (Hymenoptera: Eulophidae)

Abstract Melittobia are gregarious ectoparasitoid wasps that primarily attack various solitary bees and wasps. Characterized by high levels of inbreeding and an extremely female-biased sex ratio, these wasps appear to satisfy Hamilton's criteria for local mate competition. However, previous studies of sex ratio have failed to take into account an important aspect of Melittobia life history, namely that every clutch represents the combined reproductive output of the initial foundress female plus as many as 37 non-disperser short-winged daughters. Melittobia femorata Dahms is unique among the 13 species of Melittobia in that adults emerge as two temporally distinct clutches. While the overall sex ratio of the combined progeny from both clutches (0.025 ± 0.01) is typical for that for other Melittobia species (between 0.02 - 0.04 for single foundress cultures of the five other species included in this study), the sex ratio for the brachypterous first clutch of M. femorata from field-parasitized hosts averaged about 10 times greater (0.303 ± 0.10). Laboratory experiments with single foundress M. femorata cultures on the same host species ( Trypoxylon politum Say) maintained at 25°C or 30°C produced smaller first clutch sizes compared to the field-infested hosts. While the number of brachypterous first clutch daughters was similar, significantly reduced first clutch sex ratios relative to field-parasitized hosts (0.07 - 0.10) were due to significantly fewer males being produced. Possible reasons for these differences and the elevated first clutch sex ratio in this species are discussed.     

Life history of Kladothrips ellobus and Oncothrips rodwayi: insight into the origin and loss of soldiers in gall-inducing thrips

1. The evolution of eusociality in Australian gall‐inducing thrips cannot be understood without comparisons among closely related solitary species. The life history of two solitary, gall‐inducing thrips, Kladothrips ellobus and Oncothrips rodwayi, was investigated, and data for solitary and eusocial species from previous studies were re‐analysed. Kladothrips ellobus is in a clade that is closely related to the eusocial species. Oncothrips rodwayi is in the same clade as the eusocial species and appears to have undergone an evolutionary loss of eusociality. It is the only galling thrips on Acacia in temperate environments. 2. The brood size of K. ellobus is eight to 23 times larger than broods of foundresses in eusocial species whereas the brood size of O. rodwayi is not significantly different from those of foundresses in eusocial species. 3. In K. ellobus, the mean sex ratio was not significantly different from parity but in O. rodwayi the mean sex ratio was 0.13 male. In O. rodwayi, 77% of females were inseminated by their brothers before dispersal, which is consistent with high levels of inbreeding in eusocial species of the same clade. Sex ratios suggest random mating in K. ellobus whereas female‐biased sex ratios in O. rodwayi are consistent with inbreeding and local mate competition. 4. Comparisons among solitary and eusocial species suggest that large brood size is an ancestral trait for eusociality in thrips, and this trait persists in solitary species as an r‐selection strategy. Soldiers may have evolved in arid environments to minimise the risks of dispersal and the costs of latency to reproduction, and to maximise gall defence. 5. Temperate conditions could have facilitated the evolutionary loss of soldiers in O. rodwayi, as there should be a shorter, safer, more predictable window period between dispersal and gall induction, reducing the period of latency to reproduction following dispersal and lowering risks of dispersal. 6. The loss of soldiers in O. rodwayi is not associated with a reversion to the large brood sizes of solitary species in ancestral lineages.     

An Inclusive Fitness-Based Exploration of the Origin of Soldiers: The Roles of Sex Ratio, Inbreeding, and Soldier Reproduction

I present an inclusive fitness model for the origin of soldiers that incorporates soldier production of males and females, in haplodiploids and diploids. In this paper, the term soldier refers to an individual that is morphologically and/or behaviorally specialized for defense. However, the model presented here can usefully be extended to other helping behaviors that are episodic in nature and that impact the colony as a whole rather than helping behavior that is directed to specific individuals. In general, the results of the model show that proto-soldier reproduction via sib-mating increases the ease with which soldiering evolves. Male haplodiploids appear the most apt to evolve soldier behavior compared to female haplodiploids and diploids. Haplodiploid females are expected to produce a greater proportion of male dispersers relative to their production of female dispersers and thereby increase the predilection in females to evolve soldiering compared to diploid populations. Application of the model to gall-forming thrips in Australia reveals that species basal to the phylogenetic branch where soldiers are inferred to have evolved show a lower threshold for soldier evolution than more derived species. This phylogenetic pattern is consistent with soldier production of male and female offspring facilitating the origin of soldiering in the social gall-forming thrips.     

A Comparative Study of Sex Ratio and Clutch Size in Gregarious Ichneumonoid Wasps

Some convincing support for sex ratio theory comes from the cross-species relationship between sex ratio and brood size in gregarious bethylid wasps (Hymenoptera: Bethylidae), in which the proportion males declines as brood size increases as predicted under local mate competition. It is unknown how widely such relationships hold within parasitoid wasps as a whole. We assemble a dataset on sex ratio and brood size for gregarious Braconidae and Ichneumonidae. Their sex ratios deviate substantially from those of bethylids; sex ratios differ widely across species; and they are not significantly related to brood size across species. Several factors explain the heterogeneity in sex ratios including across-species differences in mating system, sex determining mechanism, and sexual asymmetries in larval competition and polyembryony leading to single-sexed broods.     

COMPARATIVE ANALYSIS OF GALL MORPHOLOGY IN AUSTRALIAN GALL THRIPS: THE EVOLUTION OF EXTENDED PHENOTYPES

We used a combination of morphometric, phylogenetic, and life-history information to analyze the evolution and possible adaptive significance of gall morphology in a clade of 24 species of gall-inducing thrips (Insecta: Thysanoptera) on Australian Acacia trees. Principal components analysis revealed that galls varied in morphology along two main axes, spherical versus elongate (PC1) and general size (PC2). A high degree of conservation of gall shape on an independently derived phylogeny of the insects and the presence of nine species of Acacia each bearing two or three morphologically disparate gall forms induced by different thrips species indicate that interspecific variation in gall form is determined predominantly by the insects. Character optimization of PC1 on the phylogeny of gall thrips suggested that the ancestral gall form was a simple roll or curl. The diversification of gall form involved four main processes: (1) the convergent evolution of relatively spherical galls in two clades; (2) the evolution of small elongate and hemispherical galls in one clade; (3) the evolution of a lobed interior in a species with a spherical gall and multiple within-gall generations; and (4) the evolution of intraspecific gall polymorphism in a clade of apparent sibling species. Comparative analyses indicated that gall sphericity was associated with the presence of physogastry (foundress hyperfecundity) and that small elongate and hemispherical forms may be associated with the presence of multiple generations in a gall and, perhaps, with the presence of soldier castes. The evolution of a lobed interior in one species, which greatly increases inner surface area, coincided with the evolution of multiple generations. In the clade with intraspecific gall polymorphism in some species, patterns of intraspecific variation mirror patterns of interspecific variation within the clade as a whole. This is the first study to analyze the evolution of gall size and shape in a phylogenetic context and to investigate the life-history correlates of evolutionary changes in gall form. Taken together, our findings indicate that the main selective pressures driving the evolution of gall form in Australian gall thrips on Acacia involve inner surface area to volume relationships, which change in concert with foundress fecundity and the number of within-gall generations.     

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.     

Phylogenetics of gall-inducing thrips on Australian Acacia

Analysis of DNA sequence data from four genes ( Elongation Factor-1 α, wingless , 16S rDNA and cytochrome oxidase I ) yielded a well-resolved, well-supported phylogeny for all 21 species of gall-inducing thrips found on Australian Acacia. This phylogeny was then used to investigate the evolution of various behavioural and life history traits, and to examine the level of agreement with the taxonomy of the group. Our results suggest that there may have been a single origin of soldier castes in gall-inducing thrips. Examination of the distribution of the three primary life history strategies employed by these thrips (pupating in the gall, pupating in soil with soldier castes and pupating in soil without soldier castes) indicates that two of the strategies may have evolved as a result of factors associated with host plant affiliations or through parasite pressure. Our phylogeny does not support the existing generic classification of the group in that the genera are not monophyletic, nor does it lend itself to a clear solution to improve the classification in accordance with the phylogeny.     

Inbreeding and population structure in two pairs of cryptic fig wasp species

We used recently developed microsatellites to directly estimate inbreeding levels in two pairs of coexisting cryptic fig wasp species ('Pegoscapus hoffmeyeri sp. A and sp. B', 'P. gemellus sp. A and sp. B'). Previous tests of Hamilton's local mate competition (LMC) theory in fig wasps have used the number of dead foundresses in a fig fruit to indirectly estimate the relative contribution of each to the common brood and thereby the level of local mate competition. Further, the population level of inbreeding has been indirectly estimated using the distribution of foundress numbers across broods. Our direct genetic estimates confirmed previous assumptions that the species characterized by lower foundress numbers showed higher relative levels of inbreeding. However, there were quantitative differences between the observed level of inbreeding and the expectation based on the distribution of foundress numbers in both pollinator species associated with Ficus obtusifolia. Here, genotype compositions of broods revealed that only 23% of fruits with multiple foundresses actually contained brood from more than one foundress, thus explaining at least part of the underestimate of actual sibmating. Within the four wasp species there was no evidence for genetic differentiation among the wasp populations sampled from different trees across 20 km and from different points in time. Further, no genotypic disequilibrium was detected within any of the species. Although F1 hybrids were observed between the two species pollinating F. obtusifolia, there was no evidence of genetic introgression. Finally, we found that 11% of the sons of allospecifically mated mothers were diploid hybrids suggesting a break down of the sex determination system in hybrids.     

Simultaneous failure of two sex-allocation invariants: implications for sex-ratio variation within and between populations

Local mate competition (LMC) occurs when male relatives compete for mating opportunities, and this may favour the evolution of female-biased sex allocation. LMC theory is among the most well developed and empirically supported topics in behavioural ecology, clarifies links between kin selection, group selection and game theory, and provides among the best quantitative evidence for Darwinian adaptation in the natural world. Two striking invariants arise from this body of work: the number of sons produced by each female is independent of both female fecundity and also the rate of female dispersal. Both of these invariants have stimulated a great deal of theoretical and empirical research. Here, we show that both of these invariants break down when variation in female fecundity and limited female dispersal are considered in conjunction. Specifically, limited dispersal of females following mating leads to local resource competition (LRC) between female relatives for breeding opportunities, and the daughters of high-fecundity mothers experience such LRC more strongly than do those of low-fecundity mothers. Accordingly, high-fecundity mothers are favoured to invest relatively more in sons, while low-fecundity mothers are favoured to invest relatively more in daughters, and the overall sex ratio of the population sex ratio becomes more female biased as a result.