Offspring sex ratio response to host size in the parasitoid wasp Spalangia endius

The host size model, an adaptive model for maternal manipulation of offspring sex ratio, was examined for the parasitoid wasp Spalangia endius. In a Florida strain, as the model predicts, daughters emerged from larger hosts than sons, but only when mothers received both small and large hosts simultaneously. The pattern appeared to result from the mother's ovipositional choice and not from differential mortality of the sexes during development. If sex ratio manipulation is adaptive in the Florida strain, it appears to be through a benefit to daughters of developing on large hosts rather than through a benefit to sons of developing on small hosts. Both female and male parasitoids were larger when they developed on larger hosts. For females, developing on a larger host (1) increased offspring production, except for the largest hosts, (2) increased longevity, (3) lengthened development, and (4) had no effect on wing loading. For males, development on a larger host had no effect on any measure of male fitness – mating success, longevity, development duration, or wing loading. In contrast, a strain from India showed no difference in the size of hosts from which daughters versus sons emerged, although both female and male parasitoids were larger when they developed on larger hosts. These results together with previous studies of Spalangia reveal no consistent connection between host-size-dependent sex ratio and host-size-dependent parasitoid size among strains of S. endius or among species of Spalangia. Received: 28 October 1998 / Received in revised form: 20 May 1999 / Accepted: 30 May 1999     

Sex ratio and oviposition responses to host age and the fitness consequences to mother and offspring in the parasitoid wasp Spalangia endius

In the parasitoid wasp Spalangia endius more offspring and a greater proportion of daughters were oviposited in, and emerged from 0-day-old versus 3-day-old hosts. Offspring that developed on the younger hosts (1) were larger at adulthood, (2) developed more quickly, (3) had higher survivorship to adulthood, and (4) were more often able to chew their way out of the host. Sons and daughters did not differ in how host age affected their size, development rate, or survivorship. The greater proportion of daughters from the younger hosts may be adaptive, as described by the host quality model (a variant of the Trivers and Willard hypothesis). It is adaptive if greater size or more rapid development has a more positive effect on a daughter’s than a son’s fitness and the positive effect is large enough to compensate for sons being trapped disproportionately to daughters in the older hosts. Despite greater success at drilling the younger hosts, mothers did not try to drill them sooner or more often. Having previously oviposited on the older rather than the younger hosts had no detrimental effect on the mother’s subsequent longevity or offspring production. Received: 8 March 2000 / Revised: 9 June 2000 / Accepted: 24 June 2000     

Sex ratio and host size in a parasitoid wasp

Summary Parasitoid wasps often lay male eggs in small hosts and female eggs in larger hosts. The selective advantage of this strategy can be explained by assuming wasp fitness increases with host size and that this fitness increase is greater in females than in males. I conducted experiments to test a model based on this explanation and found the results generally supported the model with one exception; unlike what the model assumed, these wasps were unable to adjust their offspring sex ratios in each generation to different host size distributions. This finding suggests an alternate view as to how selection might operate in the evolution of parasitoid sex ratios.     

Host choice and offspring sex allocation in a solitary parasitic wasp

Summary Females of the parasitic wasp Antrocephalus pandens can detect differences in the quality of their hosts (pupae of Corcyra cephalonica, a stored-product moth) and allocate offspring of either sex accordingly. Larger and younger hosts are accepted more often in both dead and live hosts; more female offspring emerge from the perceived better hosts, while more males emerge from the smaller, older ones. These patterns are consistent with a sex allocation strategy by the mother, since females from a given size host tend to be larger than males and larger females produce more eggs. However, when wasps lay their eggs in groups of hosts of different size and age rather than encountering them one at a time, no difference in number or sex ratio of offspring is detected between groups. This result and evidence from the change in offspring sex ratio with female age and with numbers of females foraging on a group of hosts are interpreted and discussed in the context of sex allocation (Charnov 1979) and local mate competition (LMC, Hamilton 1967) theories.     

Mind the gap: the ratio of yolk androgens and antioxidants varies between sons and daughters dependent on paternal attractiveness

Females are expected to partition resources between offspring in a context-dependent way to maximise total fitness returns from a reproductive attempt. Female zebra finches (Taeniopygia guttata) vary the allocation of yolk androgens and antioxidants among offspring. Importantly, the balance between androgens and antioxidants in yolks may be more important than their independent absolute amounts in terms of fitness consequences for developing young. Therefore, we tested whether the relative allocation of these two resources in yolks varies according to either the Trivers–Willard, positive or compensatory maternal investment hypothesis. We manipulated male attractiveness using coloured leg bands (red-banded males appear attractive; green-banded males, unattractive) and measured yolk androgens and antioxidants in each egg, egg sex, clutch sex ratio and female condition. While female zebra finches manipulated the balance of androgens and antioxidants within and between clutches in response to mate attractiveness, offspring sex and their own condition, they did not do so in a way that consistently followed any of the hypotheses. Mothers paired with unattractive males allocated a larger antioxidant/androgen ratio to daughters than sons. This pattern was reversed when paired to an attractive male; sons received a larger antioxidant/androgen ratio than daughters. We also found offspring sex ratio decreased with increasing female condition for unattractive males, but not for attractive males. However, without knowing the fitness consequences of the balance of different egg constituents, it is difficult to interpret the patterns consistently in terms of the Trivers–Willard, compensatory and positive investment hypotheses.     

Optimal investment in sons and daughters when parents do not know the sex of their offspring

Optimal parental investment usually differs depending on the sex of the offspring. However, parents in most organisms cannot discriminate the sex of their young until those young are energetically independent. In a species with physical male–male competition, males are often larger and usually develop sexual ornaments, so male offspring are often more costly to produce. However, Onthophagus dung beetles (Coleoptera; Scarabaeidae) are highly dimorphic in secondary sexual characters, but sexually monomorphic in body size, despite strong male–male competition for mates. We demonstrate that because parents provide all resources required by their offspring before adulthood, O. atripennis exhibits no sexual size dimorphism irrespective of sexual selection pressure favoring sexual dimorphism. By constructing a graphic model with three fitness curves (for sons, daughters, and expected fitness return for parents), we demonstrate that natural selection favors parents that provide both sons and daughters with the optimal amount of investment for sons, which is far greater than that for daughters. This is because the cost of producing small sons, that are unable to compete for mates, is far greater than the cost of producing daughters that are larger than necessary. This theoretical prediction can explain sexual dimorphism without sexual size dimorphism, widely observed in species with crucial parental care such as dung beetles and leaf-rolling beetles, and may provide an insight into the enigmatic relationship between sexual size dimorphism and sexual dimorphism.     

Cooperatively breeding superb fairy-wrens show no facultative manipulation of offspring sex ratio despite plausible benefits

We report a long-term study of offspring sex ratios in the cooperatively breeding superb fairy-wren Malurus cyaneus. Detailed study of this species had revealed a suite of potentially strong selection pressures on the sex ratio. First, females gain substantial fitness benefits from the presence of helpers; so females without male helpers would benefit from any strategy that increased the probability of recruiting help, such as overproduction of sons (local resource enhancement hypothesis), but large numbers of helper males compete among themselves, favouring the production of daughters (local resource competition). Second, daughters fledged early in the season have far greater chances of recruitment to the breeding population than late-fledged daughters, so mothers would benefit from production of daughters early in the breeding season (early bird hypothesis). Third, extra-group mate choice imposes strong sexual selection on males, suggesting that females mating with attractive sires could benefit from investing in sons (sexual selection hypothesis). However, the predictions from these and other sex ratio hypotheses were rejected. The only convincing evidence for manipulation of the sex ratio was a slight bias towards sons (11 sons to 10 daughters) that occurred regardless of context. This result does not support current theory.     

Impacts of flight distance on sex ratio and resource allocation to offspring in the leafcutter bee, Megachile rotundata

Fisher's theoretical prediction of equal investment in each sex for a panmictic population (The genetical theory of natural selection. Clarendon, Oxford, 1930) can be altered by a number of factors. For example, the sex ratio theory predicts variation in equal investment in each sex when the maternal fitness gains from increased investment differ between sexes. Changing sex allocation because of changing payoffs may result from different ecological situations, such as foraging conditions. We investigated the impact of foraging travel cost on relative investment in sons vs daughters. Field studies were carried out with the central-place-foraging leafcutter bee Megachile rotundata (Fabricius), which has smaller males than females. Therefore, less investment is required to produce a viable son compared with a daughter. We found that with increased flight distance to resources, females produced a greater proportion of sons. Females also invested fewer resources in individual sons and daughters and produced fewer offspring with increased flight distance.     

Local mate competition in the solitary parasitoid wasp <Emphasis Type="Italic">Ooencyrtus kuvanae</Emphasis>

Local mate competition (LMC) occurs when brothers compete with each other for mating opportunities, resulting in selection for a female-biased sex ratio within local groups. If multiple females oviposit in the same patch, their sons compete for mating opportunities with non-brothers. Females, in the presence of other females, should thus produce relatively more sons. Sex ratio theory also predicts a more female-biased sex ratio when ovipositing females are genetically related, and sex-ratio responses to foundress size if it differentially affects fitness gains from sons versus daughters. The mating system of the parasitoid wasp Ooencyrtus kuvanae meets assumptions of LMC. Females insert a single egg into each accessible egg of gypsy moth, Lymantria dispar, host egg masses. Wasps complete development inside host eggs and emerge en masse, as sexually mature adults, resulting in intense competition among brothers. We tested the hypothesis that O. kuvanae exhibits LMC by manipulating the number of wasp foundresses on egg masses with identical numbers of eggs. As predicted by LMC theory, with increasing numbers of wasp foundresses on an egg mass, the proportions of emerging sons increased. In contrast, the presence of a sibling compared to a non-sibling female during oviposition, or the size of a female, did not affect the number or sex ratio of offspring produced. The O. kuvanae system differs from others in that larvae do not compete for local resources and thus do not distort the sex ratio in favor of sons. With no resource competition among O. kuvanae larvae, the sex ratio of emergent son and daughter wasps is due entirely to the sex allocation by ovipositing wasp foundresses on host egg masses.     

No evidence for offspring sex-ratio adjustment to social or environmental conditions in cooperatively breeding purple-crowned fairy-wrens

When fitness returns or production costs vary between male and female offspring, selection is expected to favor females that adjust offspring sex ratio accordingly. However, to what extent vertebrates can do so is the subject of ongoing debate. Here, we explore primary sex ratios in 125 broods of cooperatively breeding purple-crowned fairy-wrens Malurus coronatus. We expected that females might adjust offspring sex ratio because this passerine species experiences considerable variation in social and environmental conditions. (1) However, although helpers substantially increase parental fitness, females (particularly in pairs and small groups) did not overproduce philopatric males (helper-repayment hypothesis). (2) Sex-ratio adjustment based on competition among individuals (helper-competition hypothesis) did not conceal helper-repayment effects or drive sex allocation on its own: while high-quality territories can accommodate more birds, brood sex ratios were independent of territory quality, alone or in interaction with group size. (3) Additionally, males are larger than females and are possibly more costly to produce (costly sex hypothesis), and (4) female offspring may benefit more from long-term effects of favorable conditions early in life (Trivers–Willard hypothesis). Nonetheless, large seasonal variation in food abundance was not associated with a consistent skew in primary sex ratios. Thus, overall, our results did not support the main hypotheses of adaptive sex-ratio adjustment in M. coronatus. We discuss that long-term differential costs and benefits may be insufficient to drive evolution of primary sex-ratio manipulation by M. coronatus females. More investigation is therefore needed to determine the general required sex differences in long-term fitness returns for mechanisms of primary sex-ratio manipulation to evolve.     

Female egg investment in relation to male sexual traits and the potential for transgenerational effects in sexual selection

Life-history theory predicts that individuals should increase their reproductive effort when the fitness return from reproduction is high. Females mated with high-quality males are therefore expected to have higher investment than females mated with low-quality males, which could bias estimates of paternal effects. Investigating the traits females use in their allocation decisions and the aspects of reproduction that are altered is essential for understanding how sexual selection is affected. We studied the potential for differential female allocation in a captive population of a precocial bird, the Chinese quail, Coturnix chinensis. Females paired with males with large sexual ornaments laid larger, but not more, eggs than females paired with males with small sexual ornaments. Furthermore, female egg mass was also significantly positively affected by male testis size, probably via some unknown effect of testis size on male phenotype. Testis size and ornament size were not correlated. Thus, both primary and secondary male sexual traits could be important components of female allocation decisions. Experimental manipulation of hormone levels during embryonic development showed that both male and female traits influencing female egg size were sensitive to early hormone exposure. Differences in prenatal hormone exposure as a result of maternal steroid allocation to eggs may explain some of the variation in reproductive success among individuals, with important implications for non-genetic transgenerational effects in sexual selection.Communicated by C. Brown     

Purification of multiple vitellogenins in grey mullet (<Emphasis Type="Italic">Mugil cephalus</Emphasis>)

Coralliophila abbreviata (Lamarck) is a corallivorous gastropod that lives and feeds on several species of scleractinian coral in the Western Atlantic and Caribbean. Previous studies of C. abbreviata have revealed that snails on branching acroporid corals are larger and consume more tissue than those on massive and plating corals. To ascertain whether snail life-history and fitness are differentially affected by the coral host, an analysis of the age structure and female reproductive output of snail populations on three coral host taxa (Acropora palmata, Diploria spp., and Montastraea spp.) was conducted at four shallow (2–7 m depth) reef sites off Key Largo, Florida in June through August, 2004. Snails were, on average, almost twice as large on A. palmata than on Diploria spp. and Montastraea spp., averaging 30.3 mm shell length, compared to 17.2 and 17.6 mm, respectively. Brood size increased as a power function with female shell length. Females on A. palmata were significantly larger than females on the other two hosts and, therefore, produced more offspring per female. The number of growth striae on the inner surface of the operculum was used to estimate snail age. Estimates of growth rate were obtained by fitting the Gompertz growth function to size-at-age plots and mortality was estimated using growth parameters and size-frequency data. The data suggest that C. abbreviata inhabiting A. palmata are larger than on alternative hosts due to a combination of a faster growth rate and longer life-span. The species is believed to be a protandrous hermaphrodite. The timing of sex change varied among hosts; snails on A. palmata changed sex later at larger sizes relative to those on the other two hosts. Based on these results, it seems probable that C. abbreviata has developed reaction norms for life-history traits, allowing snails to adjust and maximize fitness in the different environments associated with various coral hosts.     

Competition with flies promotes communal breeding in the burying beetle,Nicrophorus tomentosus

Communal breeding through nest-sharing may benefit cooperating individuals indirectly, in increased inclusive fitness, or directly, when environmental constraints reduce the fitness of solitary breeders. Burying beetles provide extensive parental care and can breed either in pairs or in larger groups of unrelated males and females. Parentage of communally-reared broods is usually shared but is skewed in favor of the individuals of each sex that provide longer care. Females provide care longer than males, and two females are more likely to remain together in the brood chamber than two males are. Flies and other burying beetles are the major competitors for carcasses and this study suggests that it is competition with flies that promotes communal breeding inNicrophorus tomentosus On medium-size carcasses (35–40 g) the presence or absence of oviposition by flies had a significant effect on the size of the brood reared, and on large carcasses (55–60 g) the number of beetles present, two or four, had a significant effect on brood size. On both medium and large carcasses, pairs rearing broods on flyblown carcasses had fewer young than pairs on clean carcasses or foursomes on flyblown carcasses. There was a strong trend for an interaction effect between number of beetles and competition with flies (Table 1). Duration of parental care was not affected by competition with flies except for that of the first male to depart, which provided care longer on flyblown carcasses (Table 2). Pairs and foursomes were equally able to defend the carcass and brood from conspecific intruders and from larger intrudingNicrophorus orbicollis (Table 3).     

Modification of hosts' behavior by a parasite: field evidence for adaptive manipulation

Parasites relying on trophic transmission to complete their life cycles often induce modifications of their host's behavior in ways that may increase their susceptibility to predation by final hosts. These modifications have often been interpreted as parasite adaptations, but very few studies have demonstrated that host manipulation has fitness benefits for the parasite. The aim of the present study was to address the adaptive significance of parasite manipulation by coupling observations of behavioral manipulation to estimates of trophic transmission to the definitive host in the natural environment. We show that the acanthocephalan parasite Pomphorhynchus laevis manipulates the drifting behavior of one of its intermediate hosts, the amphipod Gammarus pulex, but not of a sympatric host, the introduced amphipod Gammarus roeseli. We found a 26.3-28.3 times higher proportion of infected G. pulex in the stomach content of one of the definitive hosts of P. laevis, the bullhead Cottus gobio, than in the benthos. No such trend was observed for G. roeseli. The bell-shaped curve of mean parasite abundance (MPA) relative to host size observed in G. pulex also supported an increased predation mortality of P. laevis-infected individuals compared to uninfected amphipods. Again, no such pattern was observed in G. roeseli. Furthermore, our results indicate that the modifications induced by P. laevis are specific to the definitive host and do not increase the risk of predation by inappropriate hosts, here the adult edible frog Rana esculenta. Overall, our study is original in that it establishes, under field conditions, a direct link between parasitic manipulation and increased transmission to the definitive host, and more importantly, identifies the specificity of the manipulation both in the intermediate host species and toward the definitive host.     

Disappearance and dispersal of Spermophilus elegans juveniles in relation to behavior

Summary Patterns of disappearance and dispersal of Spermophilus elegans juveniles during the first 6-weeks postemergence were compared for 1977 and 1978 and related to quantitative and qualitative changes in social interaction involving juveniles.Juvenile disappearance (emigration or mortality) and dispersal within the study site varied between the sexes within and between years. Female disappearance and dispersal were significantly greater in 1977, and male losses in 1978 significantly exceeded male losses in 1977. Greater female loss in 1977 resulted in total male — female losses being equivalent, whereas in 1978 juvenile loss was strongly biased toward males by the end of the 6-week period.Greater female loss in 1977 was attributed primarily to increased aggression between female juveniles in that year because of larger average litter size with more females per litter. Increased disappearance of males in 1978 showed no correlation with litter size or relative increase in number of males per litter. Male young interacted with individuals of several age/sex classes, and a possible behavioral influence on male disappearance was increased aggressiveness by yearling males toward juvenile males in 1978.Behavior appeared to act as a proximate factor in juvenile disappearance and dispersal, and the observed differences between how male and female juveniles interacted in 1977 and 1978 were hypothesized to reflect the operation of different selective pressures to increase individual male or female fitness.     

Brood sex ratios, female harem status and resources for nestling provisioning in the great reed warbler (Acrocephalus arundinaceus)

The theory of parental investment and brood sex ratio manipulation predicts that parents should invest in the more costly sex during conditions when resources are abundant. In the polygynous great reed warbler, Acrocephalus arundinaceus, females of primary harem status have more resources for nestling provisioning than secondary females, because polygynous males predominantly assist the primary female whereas the secondary female has to feed her young alone. Sons weigh significantly more than daughters, and are hence likely to be the more costly sex. In the present study, we measured the brood sex ratio when the chicks were 9 days old, i.e. the fledging sex ratio. As expected from theory, we found that female great reed warblers of primary status had a higher proportion of sons in their broods than females of lower (secondary) harem status. This pattern is in accordance with the results from two other species of marsh-nesting polygynous birds, the oriental reed warbler, Acrocephalus orientalis, and the yellow-headed blackbird Xanthocephalus xanthocephalus. As in the oriental reed warbler, we found that great reed warbler males increased their share of parental care as the proportion of sons in the brood increased. We did not find any difference in fitness of sons and daughters raised in primary and secondary nests. The occurrence of adaptive sex ratio manipulations in birds has been questioned, and it is therefore important that three studies of polygynous bird species, including our own, have demonstrated the same pattern of a male-biased offspring sex ratio in primary compared with secondary nests. Received: 1 June 1999 / Received in revised form: 10 January 2000 / Accepted: 12 February 2000     

Learning and natal host influence host preference,handling time and sex allocation behaviour in a pupal parasitoid

The host choice and sex allocation decisions of a foraging female parasitoid will have an enormous influence on the life-history characteristics of her offspring. The pteromalid Pachycrepoideus vindemiae is a generalist idiobiont pupal parasitoid of many species of cyclorrhaphous Diptera. Wasps reared in Musca domestica were larger, had higher attack rates and greater male mating success than those reared in Drosophila melanogaster. In no-choice situations, na?ve female P. vindemiae took significantly less time to accept hosts conspecific with their natal host. Parasitoids that emerged from M. domestica pupae spent similar amounts of time ovipositing in both D. melanogaster and M. domestica. Those parasitoids that had emerged from D. melanogaster spent significantly longer attacking M. domestica pupae. The host choice behaviour of female P. vindemiae was influenced by an interaction between natal host and experience. Female P. vindemiae reared in M. domestica only showed a preference among hosts when allowed to gain experience attacking M. domestica, preferentially attacking that species. Similarly, female parasitoids reared on D. melanogaster only showed a preference among hosts when allowed to gain experience attacking D. melanogaster, again preferentially attacking that species. Wasp natal host also influenced sex allocation behaviour. While wasps from both hosts oviposited more females in the larger host, M. domestica, wasps that emerged from M. domestica had significantly more male-biased offspring sex ratios. These results indicate the importance of learning and natal host size in determining P. vindemiae attack rates, mating success, host preference and sex allocation behaviour, all critical components of parasitoid fitness. Electronic Publication     

Swarming and mating behavior of a mayfly Baetis bicaudatus suggest stabilizing selection for male body size

Large size often confers a fitness advantage to female insects because fecundity increases with body size. However, the fitness benefits of large size for male insects are less clear. We investigated the mating behavior of the mayfly Baetis bicaudatus to determine whether the probability of male mating success increased with body size. Males formed mating aggregations (swarms) ranging from a few to hundreds of individuals, 1-4 m above the ground for about 1.5-2 h in the early morning. Females that flew near swarms were grabbed by males, pairs dropped to the vegetation where they mated and then flew off individually. Some marked males returned to swarms 1, 2 or 3 days after marking. Larger males swarmed near spruce trees at the edges of meadows, but the probability of copulating was not a function of male body size (no large male advantage). Furthermore, the potential fitness advantage of mating with larger, more fecund females was not greater for large males (no size-assortative mating). However, the sizes of copulating males were significantly less variable than those of non-mating males collected at random in swarms. Intermediate male size may be optimal during mating because of trade-offs between flight agility and longevity or competitive ability. Results of this study are consistent with the hypotheses that there is stabilizing selection on adult male body size during mating, and that male body size in this species may be influenced more by selection pressures acting on larvae than on adults.     

Offspring sex ratio variation in the bridled nailtail wallaby, Onychogalea fraenata

The bridled nailtail wallaby is a sexually size dimorphic, promiscuous, solitary macropod. Sex ratios of pouch young were studied at two sites over 3 years, beginning with 14 months of severe drought. Females that were in better condition were more likely to have sons, and condition was dependent on body size. Females at one site were heavier, were consequently in better condition, and produced more sons than females at the other site. Females that declined in condition had more daughters during the most severe part of the drought than females that maintained condition, but endoparasite infection did not affect the pouch young sex ratio. Age also appeared to affect sex ratio adjustment, because weight was strongly influenced by age. Sex ratio bias was not caused by early offspring mortality, but occurred at conception. Mothers did not appear to bias energy expenditure on sons or daughters; males and females did not differ in condition at the end of pouch life. Pouch young sex ratio variation was most consistent with the Trivers-Willard hypothesis, but could also have been influenced by local resource competition, since sons dispersed further than daughters. Offspring condition was related to survival, and was correlated with maternal condition. Received: 14 April 1998 / Accepted after revision: 10 November 1998     

Parental investment and the secondary sex ratio in northern elephant seals

Summary Data on northern elephant seals, Mirounga angustirostris, bearing on sex ratio theory were collected at Año Nuevo, California, and other Californian and Mexican Islands, during the period 1967 to 1988. The mass of males exceeded that of females by 7–8% at birth and at weaning. The sex ratio was biased to males at birth (51.2%) and was near unity at weaning (49.6% males). The sex ratio did not vary as a function of maternal age or maternal mass except in 6-year-old females, who produced significantly more males. Although sons cost more to rear in energetic terms than daughters, and mothers were more successful weaning the latter, the sex of the pup reared exerted no significant effect on the mother's reproductive performance the following year or on her subsequent survival. These data suggest that parents invest equally in sons and daughters when investment is measured in terms of future reproduction (Fisher 1930) and provide no support for the theory of adaptive shifts in sex ratio (Trivers and Willard 1973). The small sex difference in mass due to maternal effort reflects the fact that females fast during lactation and all energy transferred is from limited body stores. Because of these circumstances, selection for superior condition at the end of the period of parental investment may act more strongly on pups, who have the opportunity to steal milk, than on their mothers.