Sex allocation in haplodiploids is mediated by egg size: evidence in the spider mite Tetranychus urticae Koch

Haplodiploid species display extraordinary sex ratios. However, a differential investment in male and female offspring might also be achieved by a differential provisioning of eggs, as observed in birds and lizards. We investigated this hypothesis in the haplodiploid spider mite Tetranychus urticae, which displays highly female-biased sex ratios. We show that egg size significantly determines not only larval size, juvenile survival and adult size, but also fertilization probability, as in marine invertebrates with external fertilization, so that female (fertilized) eggs are significantly larger than male (unfertilized) eggs. Moreover, females with on average larger eggs before fertilization produce a more female-biased sex ratio afterwards. Egg size thus mediates sex-specific egg provisioning, sex and offspring sex ratio. Finally, sex-specific egg provisioning has another major consequence: male eggs produced by mated mothers are smaller than male eggs produced by virgins, and this size difference persists in adults. Virgin females might thus have a (male) fitness advantage over mated females.     

Sex-ratio adjustment when relatives interact: a test of constraints on adaptation

Studies of sex allocation offer excellent opportunities for examining the constraints and limits on adaptation. A major topic of debate within this field concerns the extent to which the ability of individuals to adaptively manipulate their offspring sex ratio is determined by constraints such as the method of sex determination. We address this problem by comparing the extent of sex-ratio adjustment across taxa with different methods of sex determination, under the common selective scenario of interactions between relatives. These interactions comprise the following: local resource competition (LRC), local mate competition (LMC), and local resource enhancement (LRE). We found that: (1) species with supposedly constraining methods of sex determination showed consistent sex-ratio adjustment in the predicted direction; (2) vertebrates with chromosomal sex determination (CSD) showed less adjustment then haplodiploid invertebrates; (3) invertebrates with possibly constraining sex-determination mechanisms (CSD and pseudo-arrhenotoky) did not show less adjustment then haplodiploid invertebrates; (4) greater sex-ratio adjustment was seen in response to LRC and LMC than LRE; (5) greater sex-ratio adjustment was seen in response to interactions between relatives (LRC, LMC, and LRE) compared to responses to other environmental factors. Our results also illustrate the problem that sex-determination mechanism and selective pressure are confounded across taxa because vertebrates with CSD are influenced primarily by LRE whereas invertebrates are influenced by LRC and LMC. Overall, our analyses suggest that sex-allocation theory needs to consider simultaneously the influence of variable selection pressures and variable constraints when applying general theory to specific cases.     

Genetics of decayed sexual traits in a parasitoid wasp with endosymbiont-induced asexuality

Trait decay may occur when selective pressures shift, owing to changes in environment or life style, rendering formerly adaptive traits non-functional or even maladaptive. It remains largely unknown if such decay would stem from multiple mutations with small effects or rather involve few loci with major phenotypic effects. Here, we investigate the decay of female sexual traits, and the genetic causes thereof, in a transition from haplodiploid sexual reproduction to endosymbiont-induced asexual reproduction in the parasitoid wasp Asobara japonica. We take advantage of the fact that asexual females cured of their endosymbionts produce sons instead of daughters, and that these sons can be crossed with sexual females. By combining behavioral experiments with crosses designed to introgress alleles from the asexual into the sexual genome, we found that sexual attractiveness, mating, egg fertilization and plastic adjustment of offspring sex ratio (in response to variation in local mate competition) are decayed in asexual A. japonica females. Furthermore, introgression experiments revealed that the propensity for cured asexual females to produce only sons (because of decayed sexual attractiveness, mating behavior and/or egg fertilization) is likely caused by recessive genetic effects at a single locus. Recessive effects were also found to cause decay of plastic sex-ratio adjustment under variable levels of local mate competition. Our results suggest that few recessive mutations drive decay of female sexual traits, at least in asexual species deriving from haplodiploid sexual ancestors.     

Experimental analysis of a paternally inherited extrachromosomal factor

Virtually all known cases of extrachromosomal inheritance involve cytoplasmic inheritance through the maternal line. Recently, a paternally transmitted factor that causes the production of all-male families has been discovered in a parasitic wasp. The wasp has haplodiploid sex determination: male offspring are haploid and usually develop from unfertilized eggs, whereas females are diploid and usually develop from fertilized eggs. It has been postulated that this paternal sex-ratio factor (psr) is either (1) an infectious agent (a venereal disease) that is transmitted to the female reproductive tract during copulation with an infected male and, subsequently, causes all-male families or (2) a male cytoplasmic factor that is transmitted by sperm to eggs upon egg fertilization and, somehow, causes loss of the paternal set of chromosomes.—Experimental evidence is presented which shows that the factor requires egg fertilization for transmission to the next generation; therefore, it is likely to be a cytoplasmic factor. Significant potential intragenomic conflict results from the presence of this factor and two other sex-ratio distorters in this wasp species.     

Virgin wasps develop ovaries on par with mated females, but lay fewer eggs

In the primitively eusocial wasp Ropalidia marginata, mating is not necessary for a female wasp to develop her ovaries, lay eggs, and even to become the sole egg layer of her colony despite the presence of other mated nestmates. Here, we show that virgin wasps do not differ from their mated counterparts in the extent and rapidity of their ovarian development, in the proportion of individuals that build a nest and laid eggs, and in the time taken to do so. However, a significantly larger proportion of virgin females showed resorbing oocytes, and laid fewer eggs as compared to mated individuals. Thus, virgin females have the ability to develop ovaries and lay eggs but also to refrain from necessarily laying all mature eggs produced, before mating opportunities arise. This dual ability would be adaptive in haplodiploid, tropical species with perennial nesting cycles and frequent opportunities for workers to become replacement queens or solitary nest foundresses throughout the year.     

Female body size, fecundity parameters and foundation of new colonies in Anelosimus jabaquara (Araneae, Theridiidae)

Summary. As in other social spider species, subadult Anelosimus jabaquara females found new colonies after solitary dispersal. Some individuals, however, usually remain and reproduce in their natal nests. To test the hypothesis that large females disperse more often than smaller ones, we compared the body size of A. jabaquara females that remained in their natal colonies with those that left to build solitary webs. We also compared clutch size, egg diameter, total egg volume and spiderling size in both conditions. Emigrating females were significantly larger and laid larger clutches. The smaller females that had not dispersed laid significantly larger eggs, although their total egg volume was lower. Spiderlings of solitary females were smaller and had a smaller range of size variation than those from colonies. We discuss the implications of these results in terms of costs and benefits of dispersion for spiders in different nutritional conditions.     

Direct and indirect effects of imidacloprid on fecundity and abundance of Eurytetranychus buxi (Acari: Tetranychidae) on boxwoods

Populations of spider mites often reach high levels on urban plants. In many cases, insecticide applications targeting other herbivores trigger outbreaks of spider mites. Recently, elevated populations of spider mites on a diversity of plants in urban landscapes have been associated with applications of imidacloprid, a neonicotinoid insecticide. Imidacloprid has also been linked to increased fecundity in two species of spider mites. In this study, we evaluated the indirect (plant-mediated) and direct impact of imidacloprid on fecundity and longevity of Eurytetranychus buxi Garman (Acari: Tetranychidae), feeding on boxwoods, Buxus sempervirens L. Moreover, we compared the abundance of E. buxi on imidacloprid-treated and untreated boxwoods in the landscape and a greenhouse to determine if changes in the fecundity of mites exposed to imidacloprid were linked to outbreaks of E. buxi. We found that females consuming imidacloprid-treated plants laid more eggs than females feeding on untreated boxwoods, while their longevity remained unchanged. Fecundity was not affected, however, when spider mites were directly sprayed with imidacloprid and consumed foliage of untreated boxwoods. Furthermore, populations of E. buxi were greater on boxwoods treated with imidacloprid in the landscape and greenhouse. On landscape boxwoods, elevated populations of E. buxi persisted into a second year. We also observed general lack of predators of spider mites on treated and untreated boxwoods in the field suggesting that imidacloprid’s eruptive effect on E. buxi stems more from indirect changes in plant quality than from a loss of top-down regulation from E. buxi’s natural enemies.     

Factors promoting maternal trophic egg provisioning in non-eusocial animals

The adaptive function of trophic egg-laying is generally regarded as extended parental investment to the offspring. However, the evolutionary factors promoting trophic egg-laying are still unclear, because the amount of maternal investment per offspring should be ideally equal between smaller offspring with trophic eggs and larger offspring without any additional investment. Several authors have suggested that trophic egg-laying should evolve only when egg size is constrained, but this hypothesis has not been evaluated. We investigated the evolutionary mechanisms of trophic egg-laying by two different approaches. First, we evaluated morphological constraints on egg size in two sibling ladybird species, Harmonia axyridis, which is known to produce trophic eggs, and H. yedoensis. Second, we theoretically predicted the optimal proportion of trophic eggs to total eggs and egg size in relation to environmental heterogeneity, predictability of environmental quality, and investment efficiency of trophic egg consumption. The intra- and interspecific morphological comparisons suggest that morphological constraints on the evolutionary determination of egg size are weak at best in the two ladybird species. Moreover, we theoretically showed that small egg size and trophic egg-laying are favoured in heterogeneous environments when mothers cannot adjust egg size plastically. We also showed that even a small reduction in investment efficiency makes a trophic egg strategy unlikely, despite relatively high environmental predictability. We conclude that trophic egg provisioning may be a flexible maternal adaptation to a highly heterogeneous environment rather than a response to a morphological constraint on egg size.     

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.     

Influence of egg size differences within egg clutches on larval parameters in nine libellulid species (Odonata)

Abstract.  1. In libellulids, egg size differs between species and populations. There are also size differences within egg clutches of individual females.
2. Past experiments suggest that there are two different types of egg clutches in libellulids. Egg size decreases significantly during oviposition in species that perform non-contact guarding during oviposition. In contrast, in species ovipositing in tandem, egg size is randomly distributed.
3. This study deals with the possible consequences of egg size variation within the different egg clutch types. The study examined whether there is a correlation between egg development time, offspring sex or larval size and egg size.
4. The current experiments were conducted in Namibia and Germany. Five non-contact guarding and four tandem guarding libellulid species were used.
5. In some species larger eggs needed more time to develop, in some species no correlation between egg size and egg development time could be found, whereas in other species larger eggs developed faster.
6. The sex ratio was biased towards females in Leucorrhinia dubia and in Sympetrum striolatum and egg size was not associated with gender.
7. In both egg clutch types larger eggs resulted in larger larvae. In this study, evidence was found that the effects of egg size diminished with progressing larval development under good conditions. However, it is possible that the effects may have a greater influence under harsh circumstances.     

Absorption and cannibalism: do phytoseiids conserve egg resources when prey densities decline rapidly?

The number of eggs oviposited or left in the opisthosomas of dead mites (total eggs) was assessed for Metaseiulus occidentalis (Nesbitt), Neoseiulus fallacis (Garman), Typhlodromus pyri Scheuten or Amblyseius andersoni Chant when each was caged with either (1) no Tetranychus urticae Koch, (2) only odours of T. urticae, (3) ten eggs of M. occidentalis or (4) ten nymphs of M. occidentalis (T. pyri for M. occidentalis). The total eggs for the no prey versus odour tests did not differ within species; the levels were the greatest for N. fallacis > T. pyri > A. andersoni > M. occidentalis. Among treatments, egg means did not differ for M. occidentalis but they did for N. fallacis and T. pyri and similar trends were seen for A. andersoni. Egg means were usually less for mites held with ten predator nymphs than mites held with ten predator eggs or with no prey. Were adult females with nymphs absorbing rather than ovipositing their eggs or dying with them in their opisthosomas? Activity levels (walking) for adult females were no more for mites held with nymphs versus no food. The data indicated that interference by nymphs was not increasing the energy use of females and thus reducing egg levels. However, tests with ten nymphs, one egg and no adult female had egg losses from nymphal predation that could account for fewer eggs in cage tests. Overall, no evidence for absorption was found. If it occurs, it must be among younger eggs or mites exposed to less rapid prey losses than were the mites tested here; in addition, other stimuli may cause absorption. The total eggs in sticky-tape tests were greatest for N. fallacis > M. occidentalis > T. pyri > A. andersoni. Cage versus stick-tape data differed most for M. occidentalis because of cannibalism. All four mites cannibalized eggs but M. occidentalis did most rapidly and extensively. When starved, it laid all of its eggs before the other three species did. Such behaviours may enhance survival of M. occidentalis when prey become scarce.     

Do group size and laying order influence maternal deposition of testosterone in smooth-billed ani eggs?

The avian egg contains maternal hormones that affect behavior, growth, morphology, and offspring survival. Evidence to date suggests that patterns of yolk androgen deposition could provide females with a means to manipulate sibling competition and, thereby, increase their fitness. We examined yolk testosterone (T) concentrations in eggs of the smooth-billed ani (Crotophaga ani) to understand patterns of androgen deposition in eggs of this plural-breeding joint-nesting cooperatively breeding species. We tested the hatching asynchrony adjustment hypothesis, which states that increases in yolk androgen levels over the laying sequence function to mitigate the disadvantage of being a later-hatched chick in species without adaptive brood reduction. We also investigated the effect of group size on yolk T deposition to test the hypothesis that females in multi-female groups could give a competitive edge to their own chicks by depositing higher T levels in their eggs. Predictions of the hatching asynchrony adjustment hypothesis were supported in both single- and multi-female groups as yolk testosterone levels increased from early- to late-laid eggs. This suggests that ani females can influence nestling competition and chick survival by within-clutch differential T allocation. Unexpectedly, we did not observe an effect of group size on yolk T deposition. Yolk testosterone concentrations may not be a mere reflection of a female's hormonal status as female plasma circulating levels of T did not vary in the same direction as yolk T levels. Results of this study therefore support the idea that females may adaptively manipulate chick behavior through hormonal deposition in eggs.     

Climate change and sexual size dimorphism in an Arctic spider

Climate change is advancing the onset of the growing season and this is happening at a particularly fast rate in the High Arctic. However, in most species the relative fitness implications for males and females remain elusive. Here, we present data on 10 successive cohorts of the wolf spider Pardosa glacialis from Zackenberg in High-Arctic, northeast Greenland. We found marked inter-annual variation in adult body size (carapace width) and this variation was greater in females than in males. Earlier snowmelt during both years of its biennial maturation resulted in larger adult body sizes and a skew towards positive sexual size dimorphism (females bigger than males). These results illustrate the pervasive influence of climate on key life-history traits and indicate that male and female responses to climate should be investigated separately whenever possible.     

Potential of the predatory mite Phytoseius finitimus (Acari: Phytoseiidae) to feed and reproduce on greenhouse pests

Phytoseiid mites of the genus Phytoseius are natural enemies of tetranychid and eriophyid herbivorous mites mostly found on hairy plants where they feed on prey, as well as on pollen. Nevertheless, the nutritional ecology and the role of these predators in biological pest control are only rarely addressed. In the present study, we evaluated the potential of Phytoseius finitimus to feed and reproduce on three major greenhouse pests, the two-spotted spider mite, the greenhouse whitefly and the western flower thrips. Additionally, we estimated the effect of cattail pollen when provided to the predator alone or in mixed diets with prey. Contrary to thrips larvae, both spider mite larvae and whitefly crawlers sustained the development of P. finitimus. In addition, females consumed more spider mite eggs and larvae, as well as whitefly crawlers than thrips larvae, but laid eggs when feeding on all prey. When provided alone, cattail pollen sustained the development and reproduction of the predator. The addition of pollen in mixed diets with prey reduced prey consumption, though it increased the predator’s egg production. We discuss the implications of our findings for biological pest control.     

A lengthy solution to the optimal propagule size problem in the large-bodied South American freshwater turtle, <Emphasis Type="Italic">Podocnemis unifilis</Emphasis>

In oviparous vertebrates lacking parental care, resource allocation during reproduction is a major maternal effect that may enhance female fitness. In general, resource allocation strategies are expected to follow optimality models to solve the energy trade-offs between egg size and number. Such models predict that natural selection should optimize egg size while egg number is expected to vary with female size, thus maximizing offspring fitness and consequently, maternal fitness. Deviations from optimality predictions are commonly attributed to morphological constraints imposed by female size, such as reported for small-bodied turtle species. However, whether such anatomical constraints exist in smaller-bodied females within large-bodied clades remains unstudied. Here we tested whether resource allocation of the river turtle Podocnemis unifilis (a relatively smaller member of the large-bodied Podocnemididae) follows optimality theory, and found a pattern of egg elongation in smaller females that provides evidence of morphological constraints and of a reproductive trade-off with clutch size, whereas egg width supports the existence of an optimal egg size and no trade-off. Moreover, larger females laid larger clutches composed of rounder eggs, while smaller females laid fewer and relatively more elongated eggs. Elongated eggs from smaller females have larger volume relative to female size and to round eggs of equal width. We propose that elongated eggs represent a solution to a potential morphological constraint suffered by small females. Our results suggest that larger females may optimize fitness by increasing the number of eggs, while smaller females do so by producing larger eggs. Our data supports the notion that morphological constraints are likely more widespread than previously anticipated, such that they may not be exclusive of small-bodied lineages but may also exist in large-bodied lineages.     

Oviposition-site shift in phytophagous mites reflects a trade-off between predator avoidance and rainstorm resistance

Predators can reduce prey population densities by driving them to undertake costly defences. Here, we report on a remarkable example of induced antipredator defence in spider mites that enhances the risk to rainstorms. Spider mites live on the undersides of host plant leaves and usually oviposit on the leaf undersurface. When they are threatened by predatory mites, they oviposit on three-dimensional webs to avoid egg predation, although the cost of ovipositing on webs has not yet been clearly determined. We prepared bean plants harbouring spider mite (Tetranychus kanzawai) eggs on either leaf surfaces or webs and exposed them to rainstorms outdoors. We found that fewer eggs remained on webs than on leaf surfaces. We then examined the synergistic effect of wind and rain by simulating both in the laboratory. We conclude that ovipositing on webs comes at a cost, as eggs are washed off the host plants by wind and rain. This may explain why spider mite populations decrease drastically in the rainy season, although they inhibit leaf undersides where they are not directly exposed to rainfall.     

Maternal defensive behaviors of <Emphasis Type="Italic">Uloborus</Emphasis> sp. (Araneae,Uloboridae): behavioral repertoire and influence of clutch size and female size on female aggressiveness

Maternal care in spiders often involves behaviors associated with the protection of eggs and spiderlings against parasitoids and predators (including conspecifics). The females of several species have been documented to move their egg sacs away from natural enemies or to invest in active defense behaviors against web invaders, such as parasitoid wasps or araneophagic spider species, to protect their brood. In this study, we present observations of protective behavior by Uloborus sp. females carrying egg sacs. We also investigated whether brood size and female size influence female aggressive behaviors and response time against an artificial source of disturbance. Females carrying egg sacs almost immediately perceived and reacted aggressively against the artificial stimulus, whereas females without egg sacs moved away or ran to the web margins, avoiding the source of disturbance. The aggressive response was independent of clutch size and female body size, indicating that all females will risk interacting with potential agents of egg mortality. This systematic response by all females with egg sacs may be important for reducing the incidence of attack by the egg predator wasp Bathyzonus sp. (Ichneumonidae).     

Nutrient Composition of Romanomermis culicivorax in Relation to Egg Production and Metabolism

The nutrient composition of postparasitic females (newly emerged juveniles, newly molted adults, and spent adults) and eggs of Romanomermis culicivorax was studied. Throughout post-parasitic development, proteins increased and lipids decreased progressively as a proportion of the dry weight; the proportion of glycogen within the nematodes remained stable. The greatest decrease in the lipid moiety occurred during egg production. Eggs contained relatively low levels of lipids (12% dry weight), and ca. 20% of the dry weight of the eggs was unaccounted for by lipid, protein, and glycogen determinations. Chitin, mucoproteins, and peptides were present in the eggs. The fatty acid composition of nematodes remained constant during postparasitic development; eggs contained a similar profile of fatty acids as postparasites, with marginally higher content of unsaturated fatty acids. Radiotracer studies showed that the eggs could oxidize glucose and palmitic acid.     

Mating modifies female life history in a haplodiploid spider mite

Mating usually modifies females' resource allocation pattern, often as a result of conflicts between male and female partners. Can such a switch occur even in the absence of sexual conflicts? We addressed this issue in the haplodiploid spider mite Tetranychus urticae, whose biology and population structure considerably reduce conflicts between males and females over reproductive decisions. Comparing virgin and mated females, we tested the hypothesis that mated females modify their allocation pattern so as to maximize their probability of producing daughters. Mated females produced fewer but larger eggs, resulting in an overall similar reproductive effort but an increased probability of producing daughters, since in this species larger eggs are more likely to be fertilized and thus to become female. Moreover, mated females concentrated their reproduction early in life. Again, this might be a way to produce more daughters, since sperm is more abundant early in life. For virgins, spreading reproductive investment might be a way to save resources to extend life span, thus increasing their probability of encountering a sexual partner. Females with multiple opportunities for mating produced fewer eggs and a less female-biased sex ratio than once-mated females, raising the question of why multiple mating often occurs in this species.     

对叶榕传粉小蜂性比率的调节和稳定

传粉榕小蜂呈现偏雌的性比率,单双倍体性别决定系统、局域配偶竞争和近交效应被认为是调节偏雌性比率的3个主要机制。通过研究影响对叶榕传粉小蜂性比率的因素,结果表明传粉榕小蜂的偏雌性比率随局域配偶竞争强度的降低而增加;受母代雌蜂交配次数的影响,随着母代雌蜂交配次数的增加,子代的偏雌性比率逐渐降低,这一结果首次揭示了传粉榕小蜂的交配制次数对性比率的影响,并在个体水平上定量了性比率变异与雌蜂交配频次的关系。传粉小蜂的性比率与共生的非传粉小蜂的关系,非传粉小蜂的介入直接减少了传粉小蜂的数量,甚至对传粉小蜂的种群有显著影响,结果发现非传粉小蜂对传粉小蜂雌雄性的分配比率没有显著影响,传粉榕小蜂仍能正常地进行繁殖。传粉与非传粉者小蜂之间作用关系的确定,可为进一步理解两者的稳定共生的机制提供科学证据。