Condition and reproductive investment in the western mosquitofish (Gambusia affinis): little evidence for condition‐dependent sex‐biased investment

In sexually reproducing species, resources may theoretically be distributed with bias to the production of male or female offspring in response to the condition of the mother, commonly recognized as sex allocation. Using a recently characterized sex‐specific molecular marker, we tested for maternal sex allocation (i.e. maternal primary sex ratio bias and sex‐specific offspring investment) in captive laboratory‐bred western mosquitofish (Gambusia affinis) at early stages of offspring development. We found no statistical evidence to support sex allocation in G. affinis, based on maternal condition. In addition, we found little evidence for correlations between maternal condition and investment in the condition (mass) of individual offspring (of one sex or the other), although we did find that larger mothers tended to have higher fecundity.     

Mothers adjust offspring sex to match the quality of the rearing environment

Theory predicts that mothers should adjust offspring sex ratios when the expected fitness gains or rearing costs differ between sons and daughters. Recent empirical work has linked biased offspring sex ratios to environmental quality via changes in relative maternal condition. It is unclear, however, whether females can manipulate offspring sex ratios in response to environmental quality alone (i.e. independent of maternal condition). We used a balanced within-female experimental design (i.e. females bred on both low- and high-quality diets) to show that female parrot finches (Erythrura trichroa) manipulate primary offspring sex ratios to the quality of the rearing environment, and not to their own body condition and health. Individual females produced an unbiased sex ratio on high-quality diets, but over-produced sons in poor dietary conditions, even though they maintained similar condition between diet treatments. Despite the lack of sexual size dimorphism, such sex ratio adjustment is in line with predictions from sex allocation theory because nutritionally stressed foster sons were healthier, grew faster and were more likely to survive than daughters. These findings suggest that mothers may adaptively adjust offspring sex ratios to optimally match their offspring to the expected quality of the rearing environment.     

Condition-dependent sex allocation in a lek-breeding wader,the ruff (Philomachus pugnax)

Sex allocation theory predicts that females should bias the production of offspring towards the sex that will maximize maternal fitness. Here we demonstrate evidence for nonrandom sex allocation by female ruffs (Philomachus pugnax), at both the individual and population level in relation to female condition. At the population level, female condition varies significantly across 3 years and is mirrored by population sex ratio, such that in years when females are in poor condition the population offspring sex ratio is female-biased, while in years when females are in better condition there was little or no bias. In the year when females were in overall poor condition, females in better condition produced more daughters. The same relationship is also revealed by comparing the sex ratios of individual females breeding in two consecutive years in different condition. As the condition of an individual female improves (across years) she tends to produce more female offspring. Although we have shown that, as in other birds, female condition is an important determinant of sex allocation, our results also suggest that such nonrandom allocation does not occur in every year, being particularly strong in a year when females, on average, are in poorer condition. We suggest that our results are consistent with the idea that skewing the sex ratio is likely to carry a cost to females and that it is adaptive only when the fitness differential between sons and daughters is sufficient to outweigh probable costs.     

Disentangling sex allocation in a viviparous reptile with temperature‐dependent sex determination: a multifactorial approach

Females are predicted to alter sex allocation when ecological, physiological and behavioural variables have different consequences on the fitness of male and female offspring. Traditionally, tests of sex allocation have examined single causative factors, often ignoring possible interactions between multiple factors. Here, we used a multifactorial approach to examine sex allocation in the viviparous skink, Niveoscincus ocellatus. We integrated a 16‐year observational field study with a manipulative laboratory experiment to explore whether the effects of the maternal thermal environment interact with the resources available to females for reproduction to affect sex allocation decisions. We found strong effects of temperature on sex allocation in the field, with females born in warm conditions and males in cold conditions; however, this was not replicated in the laboratory. In contrast, we found no effect of female resource availability on sex allocation, either independently, or in interaction with temperature. These results corresponded with an overall lack of an effect of resource availability on any of the life history traits that we predicted would mediate the benefits of differential sex allocation in this system, suggesting that selection for sex allocation in response to resource availability may be relatively weak. Combined, these results suggest that temperature may be the predominant factor driving sex allocation in this system.     

Offspring sex ratio in the sequentially polygamous Penduline Tit Remiz pendulinus

Despite the growing literature on facultative sex-ratio adjustment in chromosomal sex-determining vertebrate taxa (birds, mammals), the consistency of results is often low between studies and species. Here, we investigate the primary and secondary offspring sex ratio of a small passerine bird, the Eurasian Penduline Tit (Remiz pendulinus) in three consecutive years. This species has a uniquely diverse breeding system, in which the male (and/or the female) abandons the nest during egg-laying, and starts a new breeding attempt. This allowed us to test (1) whether patterns of parental care, i.e., male-only care, female-only care or biparental desertion, influence offspring sex ratio, and (2) whether the offspring sex ratio is repeatable between successive clutches of males and females. Using molecular markers to sex 497 offspring in 176 broods, we show that (1) offspring sex ratio does not depend on which parent provides care, and (2) the offspring sex ratio is not repeatable between clutches of a given individual. The overall primary and secondary offspring sex ratio at a population level is not different from parity (54 ± 6% males, and 50 ± 3% (mean ± SE), respectively). We suggest that ecological and phenotypic factors, rather than individual traits of parents, may influence offspring’s sex, and conclude that there is currently no evidence for a facultative adjustment of offspring sex ratio in the Penduline Tit.     

Differential allocation in a lekking bird: females lay larger eggs and are more likely to have male chicks when they mate with less related males

The differential allocation hypothesis predicts increased investment in offspring when females mate with high-quality males. Few studies have tested whether investment varies with mate relatedness, despite evidence that non-additive gene action influences mate and offspring genetic quality. We tested whether female lekking lance-tailed manakins (Chiroxiphia lanceolata) adjust offspring sex and egg volume in response to mate attractiveness (annual reproductive success, ARS), heterozygosity and relatedness. Across 968 offspring, the probability of being male decreased with increasing parental relatedness but not father ARS or heterozygosity. This correlation tended to diminish with increasing lay-date. Across 162 offspring, egg volume correlated negatively with parental relatedness and varied with lay-date, but was unrelated to father ARS or heterozygosity. Offspring sex and egg size were unrelated to maternal age. Comparisons of maternal half-siblings in broods with no mortality produced similar results, indicating differential allocation rather than covariation between female quality and relatedness or sex-specific inbreeding depression in survival. As males suffer greater inbreeding depression, overproducing females after mating with related males may reduce fitness costs of inbreeding in a system with no inbreeding avoidance, while biasing the sex of outbred offspring towards males may maximize fitness via increased mating success of outbred sons.     

Do female parasitoid wasps recognize and adjust sex ratios to build cooperative relationships?

Sex allocation theories provide excellent opportunities to investigate not only the extent to which individuals' behaviour is adaptive, but also how they use relevant information for their decision-making. Here, we investigated whether female parasitoid wasps recognize the sex ratios of other females and adjust their laying sex ratios accordingly. Specifically, we tested the prediction of reciprocal cooperation over sex allocation. Theory predicts more female-biased (cooperative) sex ratios than in the interest of individual benefit, when a restricted number of ovipositing females interact for a long period and their offspring mate within the natal patch. This is because the female-biased sex ratio reduces competition for mates among the male offspring of the females and increases the overall reproductive productivity of the patch. In this case, females would be expected to respond to more even (noncooperative) sex ratios by others and to retaliate by also producing a less female-biased sex ratio to avoid exploitation by defectors. However, contrary to this prediction, our experiment using a sterile male technique showed that female Melittobia australica did not change their offspring sex ratios in response to the sex ratios produced by other females. This suggests that their extremely female-biased sex ratios cannot be explained by reciprocity. A meta-analysis of studies examining sex recognition ability in parasitoid wasps also did not support the predicted pattern of relevant sex ratio adjustment, suggesting that parasitoid females do not possess this ability. Here, we discuss the conditions necessary for the evolution of reciprocity linked to recognition ability.     

Facultative Sex Allocation and Sex‐Specific Offspring Survival in Barrow's Goldeneyes

Sex allocation theory predicts that females should bias their reproductive investment towards the sex generating the greatest fitness returns. The fitness of male offspring is often more dependent upon maternal investment, and therefore, high‐quality mothers should invest in sons. However, the local resource competition hypothesis postulates that when offspring quality is determined by maternal quality or when nest site and maternal quality are related, high‐quality females should invest in the philopatric sex. Waterfowl – showing male‐biased size dimorphism but female‐biased philopatry – are ideal for differentiating between these alternatives. We utilized molecular sexing methods and high‐resolution maternity tests to study the occurrence and fitness consequences of facultative sex allocation in Barrow's goldeneyes (Bucephala islandica). We determined how female structural size, body condition, nest‐site safety and timing of reproduction affected sex allocation and offspring survival. We found that the overall sex ratio was unbiased, but in line with the local resource competition hypothesis, larger females produced female‐biased broods and their broods survived better than those of smaller females. This bias occurred despite male offspring being larger and tending to have lower post‐hatching survival. The species shows strong female breeding territoriality, so the benefit of inheriting maternal quality by philopatric daughters may exceed the potential mating benefit for sons of high‐quality females.     

Exposure to the neonicotinoid imidacloprid disrupts sex allocation cue use during superparasitism in the parasitoid wasp Nasonia vitripennis

1. Neonicotinoid insecticides are potent neurotoxins of significant economic importance. However, it is clear that their use can adversely impact beneficial insects in the environment, even at low, sub‐lethal doses. 2. It has recently been shown that the neonicotinoid imidacloprid disrupts adaptive sex allocation in the parasitoid wasp Nasonia vitripennis (Walker) by limiting their ability to respond to the presence of other females on oviposition patches. In the present study, that work was extended to explore whether sex allocation when superparasitising – laying eggs on a host that has already been parasitised – is also disrupted by imidacloprid. 3. Under superparasitism, sex allocation theory predicts that females should vary their offspring sex ratio in relation to their relative clutch size. It was found that sex allocation under superparasitism in Nasonia is disrupted in a dose‐dependent manner, with exposed females producing more daughters. 4. Importantly, imidacloprid does not appear to influence the ability of females to estimate the number of eggs already present on a host, suggesting a disassociation between the sex ratio and clutch size cues. 5. The present work highlights the fitness costs to beneficial insects of exposure to neonicotinoids, but also provides clues as to how female Nasonia use information when allocating sex.     

Parental care and UV coloration in blue tits: opposite correlations in males and females between provisioning rate and mate’s coloration

Parental investment and sexually‐selected signals can be intimately related, either because the signals indicate the amount of investment that an individual is prepared to make, and hence its value as a mate (the ‘good parent process’), or because individuals are selected to vary their own investment in relation to their mate’s signals (‘differential allocation’ or ‘reproductive compensation’). Correlations between parental investment and the sexually selected signals of both an individual and its mate are therefore of central interest in sexual selection. Blue tits Cyanistes caeruleus are an ideal study species to investigate such correlations because they provide substantial amounts of biparental care and possess sexually‐selected structural UV coloration that seems to signal attractiveness in both sexes. We investigated whether feeding rates of male and female blue tits were correlated with either their own or their mate’s UV coloration, and whether any such correlation was affected by the sex ratio of the brood. We also investigated whether any such correlations were reflected in offspring phenotype. Feeding rates were not correlated with either sex of parent’s own UV coloration. However, they were correlated with the mate’s UV coloration, but in opposite directions in males and females: females had higher feeding rates when mated to bright UV males, implying differential allocation, while males had lower feeding rates when mated to bright UV females, implying reproductive compensation. These relationships were unaffected by the sex ratio of the brood. In addition, fledgling tarsus length, but not mass, was related to male UV coloration, and to female UV coloration in interaction with male age. These results suggest that both male and female attractiveness influence parental investment of the mate, and that this in turn affects offspring phenotype. We found no evidence for differential sex allocation.     

Female Cape sugarbirds (Promerops cafer) modify egg investment both for extra‐pair mates and for male tail length

The differential allocation hypothesis predicts that females should invest more in reproduction when paired with attractive males. We measured egg volume in Cape sugarbirds (Promerops cafer), a sexually dimorphic passerine, in relation to paternity of the offspring and in response to an experimental tail length treatment. We manipulated tail length, after pair formation, but before egg laying: males had their tails either shortened or left unmanipulated. Our manipulation was designed to affect female allocation in a particular breeding attempt rather than long‐term mate choice: males with shortened tails would appear to be signalling at a lower level than they should given their quality. We found that egg volume was smaller in the nests of males with experimentally shortened tails but larger when the offspring were the result of extra‐pair matings. Both these findings are consistent with the differential allocation hypothesis. We suggest that tail length may be used by females as a cue for mate quality, eliciting reduced female investment when breeding with social mates; and with males with shortened tails.     

To mate or not to mate,and subsequent host search by a haplodiploid female parasitoid wasp

Mated females of haplodiploid species can vary the sex ratio of their offspring, but virgin or sperm‐depleted females can produce only males. Depending on the costs and benefits, the theory of constrained sex allocation states that female haplodiploids may vary in their propensity to mate, with important implications for the populations’ sex ratio. Unmated female parasitoid wasps Alabagrus texanus (Braconidae) have been observed to reject matings with males, even under highly confined spatial conditions. We performed field trials to determine whether unmated female A. texanus would mate. We then compared the preferences of the resulting unmated (constrained) and mated (unconstrained) female wasps for shelters constructed and occupied by their hosts, fern moth caterpillars Herpetogramma theseusalis (Crambidae) on fern fronds. We presented the wasps with pairs of shelters collected from the field that differed in size, as well as freshness, fern species, and presence or absence of caterpillars. Unconstrained females searched small shelters more frequently than did constrained females and tended to favor senesced (old) shelters over fresher ones. They did not differ in choice between shelters on marsh and sensitive ferns or between shelters containing caterpillars and empty shelters. The preference for small shelters by the unconstrained wasps may enhance their rate of contacting favorable hosts, but the foraging regime of the constrained females should expose them to caterpillars at sites infrequently searched by the unconstrained females.     

Sex allocation and interactions between relatives in the bean beetle, Callosobruchus maculatus

When a small number of females contribute offspring to a discrete mating group, sex allocation (Local Mate Competition: LMC) theory predicts that females should bias their offspring sex ratio towards daughters, which avoids the fitness costs of their sons competing with each other. Conversely, when a large number of females contribute offspring to a patch, they are expected to invest equally in sons and daughters. Furthermore, sex ratios of species that regularly experience variable foundress numbers are closer to those predicted by LMC theory than species that encounter less variable foundress number scenarios. Due to their patterns of resource use, female Callosobruchus maculatus are likely to experience a broad range of foundress number scenarios. We carried out three experiments to test whether female C. maculatus adjust their sex ratios in response to foundress number and two other indicators of LMC: ovipositing on pre-parasitised patches and ovipositing with sisters. We did not find any evidence of the predicted sex ratio adjustment, but we did find evidence of kin biased behaviour.     

Male phenotypic quality influences offspring sex ratio in a polygynous ungulate

Evolutionary models of sex ratio adjustment applied to mammals have ignored that females may gain indirect genetic benefits from their mates. The differential allocation hypothesis (DAH) predicts that females bias the sex ratio of their offspring towards (more costly) males when breeding with an attractive male. We manipulated the number of available males during rut in a polygynous ungulate species, the reindeer (Rangifer tarandus), and found that a doubling of average male mass (and thus male attractiveness) in the breeding herd increased the proportion of male offspring from approximately 40 to 60%. Paternity analysis revealed indeed that males of high phenotypic quality sired more males, consistent with the DAH. This insight has consequences for proper management of large mammal populations. Our study suggests that harvesting, by generating a high proportion of young, small and unattractive mates, affects the secondary sex ratio due to differential allocation effects in females. Sustainable management needs to consider not only the direct demographic changes due to harvest mortality and selection, but also the components related to behavioural ecology and opportunities for female choice.     

Reproductive strategies under multiparasitism in natural populations of the parasitoid wasp Nasonia (Hymenoptera)

Parasitoid Nasonia wasps adjust their progeny sex ratio to the presence of conspecifics to optimize their fitness. Another trait under female control is the induction of offspring diapause. We analysed progeny sex ratios and the proportion of diapausing offspring of individual Nasonia females in host patches parasitized by two species, Nasonia vitripennis and Nasonia giraulti, in North American field populations using microsatellite fingerprinting. Both Nasonia species produced similar sex ratios on hosts that were co‐parasitized by their own species as by the other species, indicating that females do not distinguish between con‐ and heterospecific clutches. The sex ratios of the diapause and adult fractions of mixed broods from single females were not correlated. We found further indications that N. vitripennis females take the emergence time of the offspring into account in their sex allocation. The reproductive strategies of Nasonia under multiparasitism are largely adaptive, but also partially constrained by information.     

Better‐surviving barn swallow mothers produce more and better‐surviving sons

Sex allocation theory predicts that parents are selected to bias their progeny sex ratio (SR) toward the sex that will benefit the most from parental quality. Because parental quality may differentially affect survival of sons and daughters, a pivotal test of the adaptive value of SR adjustment is whether parents overproduce offspring of the sex that accrues larger fitness advantages from high parental quality. However, this crucial test of the long‐term fitness consequences of sex allocation decisions has seldom been performed. In this study of the barn swallow (Hirundo rustica), we showed a positive correlation between the proportion of sons and maternal annual survival. We then experimentally demonstrated that this association did not depend on the differential costs of rearing offspring of either sex. Finally, we showed that maternal lifespan positively predicted lifespan of sons but not of daughters. Because in barn swallows lifespan is a strong determinant of lifetime reproductive success, the results suggest that mothers overproduce offspring of the sex that benefits the most from maternal quality. Hence, irrespective of mechanisms causing the SR bias and mother–son covariation in lifespan, we provide strong evidence that sex allocation decisions of mothers can highly impact on their lifetime fitness.     

Nestling sex ratio is associated with both male and female attractiveness in rock sparrows

According to theory, in species in which male variance in reproductive success exceeds that of the females, sons are more costly to produce; females mated with high quality males or those in better condition should produce more sons. In monogamous species, however, the variance in the reproductive success of the two sexes is often similar and mate choice is often mutual, making predictions regarding sex allocation more difficult. In the rock sparrow Petronia petronia, both males and females have a sexually selected yellow patch on the breast, whose size correlates with individual body condition. We investigated whether the brood sex ratio co‐varies with the size of the yellow patch of the father and the mother in a sample of 173 broods (818 chicks) over 8 breeding seasons. While the size of the yellow patch of the mother and the father did not predict per se a deviation from the expected 1:1 sex ratio, brood sex ratios were predicted by the interaction of male and female yellow patch size. This result is surprising, as the ornament is sexually selected by both males and females as an indicator of quality in both sexes and should therefore be inherited by all offspring irrespective of their sex. It indirectly suggests that other sex‐specific traits associated with patch size (e.g. polygyny in males and fecundity in females) may explain the sex allocation bias observed in rock sparrows. Thus, female individual quality alone, as expressed through the size of the yellow patch, was not associated with the biases in sex ratios reported in this study. Our results rather suggest that sex allocation occurs in response to male attractiveness in interaction with female attractiveness. In other words, females tend to preferentially allocate towards the sex of the parent with more developed ornament within the pair.     

Female Control of Offspring Sex Ratios Based on Male Attractiveness in the Guppy

The sex allocation hypothesis predicts that females manipulate the offspring sex ratios according to mate attractiveness. Although there is increasing evidence to support this prediction, it is possible that paternal effects may often obscure the relationship between female control of offspring sex ratios and male attractiveness. In the present study, we examined whether females played a primary role in the manipulation their offspring sex ratios based on male attractiveness, in the guppy Poecilia reticulata, a live‐bearing fish. We excluded the paternal effects by controlling the relative sexual attractiveness of the male by presenting them to the females along with a more attractive or less attractive stimulus male. The test male was perceived to be relatively more attractive by females when it was presented along with a less attractive stimulus male, or vice versa. Subsequently, test male was mated in two different roles (relatively more and less attractive) with two females. If females were responsible for offspring sex ratio manipulation, the sex ratio of the brood would be altered on the basis of the relative attractiveness of the test male. On the other hand, if males play a primary role in offspring sex ratio manipulation, the sex ratios would not differ with the relative attractiveness of the test male. We found that females gave birth to more male‐biased broods when they mated with test males in the attractive role than when they mated with males in the less attractive role. This finding suggests that females are responsible for the manipulation of offspring sex ratios based on the attractiveness of their mates.     

TESTING MODELS OF FACULTATIVE SEX RATIO ADJUSTMENT IN THE POLLINATING FIG WASP PLATYSCAPA AWEKEI

Female hymenoptera are renowned for their ability to adjust offspring sex ratio to local mate competition. When two females share a patch, they frequently produce clutches that differ in size, the female with the larger clutch optimally producing a more female‐biased sex ratio and vice versa. Females can base their sex allocation on their own clutch size only (“self‐knowledge”) or on both females’ clutch sizes (“complete knowledge”). Few studies have genotyped offspring so that each mother's contribution can be considered separately while none has found that both sources of information are used simultaneously. We genotyped 2489 wasps from 28 figs and assigned their maternity to one of the two foundress females. We argue that likelihood is a very convenient method to compare alternative models, while fitness calculations help to appreciate the cost of maladaptation. We find that the pollinating fig wasp Platyscapa awekei simultaneously uses its own as well as the other females clutch size in allocating sex. Indeed, the complete knowledge model explains the data 36 times better than the self‐knowledge model. However, large clutches contained fewer males than the optimal predictions leading to a median selection coefficient of 0.01.     

The Influence of Maternal Quality on Brood Sex Allocation in the Small Carpenter Bee,Ceratina calcarata

In the twig‐nesting carpenter bee, Ceratina calcarata, body size is an important component of maternal quality, smaller mothers producing significantly fewer and smaller offspring than larger mothers. As mothers precisely control the sex and size of each offspring, smaller mothers might compensate by preferentially allocating their investment towards sons. We investigated whether variation in maternal quality leads to variation in sex allocation patterns. At the population level, the numerical sex ratio was 57% male‐biased (1.31 M/F), but the investment between the sexes was balanced (1.02 M/F), because females are 38% larger than males (1.28 F/M). Maternal body size explained both sex allocation pattern and size variation among offspring: larger mothers invested more in individual progeny and produced more female offspring than smaller mothers. Maternal investment in offspring of both sexes decreased throughout the season, probably as a result of increasing maternal wear and age. The exception to this pattern was the curious production of dwarf females in the first two brood cell positions. We suggest that the sex ratio distribution reflects the maternal body size distribution and a constraint on small mothers to produce small broods. This leads to male‐biased allocation by small females, to which large mothers respond by biasing their allocation towards daughters.