Egg-hatching benefits gained by polyandrous female locusts are not due to the fertilization advantage of nonsibling males

Several studies suggest that polyandrous females bias paternity in favor of unrelated males to avoid inbreeding depression. Here we tested whether the migratory locust biases sperm usage toward unrelated males by analyzing the paternity of offspring from females mated with either two siblings, or two nonsiblings, or a sibling and a nonsibling in either order. We found that the eggs of females mated only with siblings had decreased hatching success. When females mated with both a nonsibling and a sibling, egg hatchability was significantly increased. Subsequent paternity analyses found no evidence that females could avoid fertilization by sibling males. Therefore, improvement of the hatchability of eggs sired by siblings suggests that rather than biased fertilization by females toward genetically compatible or superior males, male-induced maternal effects or direct effects of male ejaculates might influence the survival of offspring sired by related males.     

Sex-specific paternal age effects on offspring quality in Drosophila melanogaster

Advanced paternal age has been repeatedly shown to modulate offspring quality via male- and/or female-driven processes, and there are theoretical reasons to expect that some of these effects can be sex-specific. For example, sex allocation theory predicts that, when mated with low-condition males, mothers should invest more in their daughters compared to their sons. This is because male fitness is generally more condition-dependent and more variable than female fitness, which makes it less risky to invest in female offspring. Here, we explore whether paternal age can affect the quality and quantity of offspring in a sex-specific way using Drosophila melanogaster as a model organism. In order to understand the contribution of male-driven processes on paternal age effects, we also measured the seminal vesicle size of young and older males and explored its relationship with reproductive success and offspring quality. Older males had lower competitive reproductive success, as expected, but there was no difference between the offspring sex ratio of young and older males. However, we found that paternal age caused an increase in offspring quality (i.e., offspring weight), and that this increase was more marked in daughters than sons. We discuss different male- and female-driven processes that may explain such sex-specific paternal age effects.     

Alloparenting experience affects future parental behavior and reproductive success in prairie voles (Microtus ochrogaster)

Various hypotheses have been proposed to explain the function of alloparental behavior in cooperatively breeding species. We examined whether alloparental experience as juveniles enhanced later parental care and reproductive success in the prairie vole (Microtus ochrogaster), a cooperatively breeding rodent. Juveniles cared for one litter of siblings (1EX), two litters of siblings (2EX) or no siblings (0EX). As adults, these individuals were mated to other 0EX, 1EX or 2EX voles, yielding seven different pair combinations, and we recorded measures of parental behaviors, reproductive success, and pup development. As juveniles, individuals caring for siblings for the first time were more alloparental; and as adults, 0EX females paired with 0EX males spent more time in the nest with their pups. Taken together, these results suggest that inexperienced animals spend more time in infant care. As parents, 1EX males spent more time licking their pups than 2EX and 0EX males. Pups with either a 1EX or 2EX parent gained weight faster than pups with 0EX parents during certain developmental periods. While inexperienced animals may spend more time in pup care, long-term benefits of alloparenting may become apparent in the display of certain, particularly important parental behaviors such as licking pups, and in faster weight gain of offspring.     

Offspring are lighter at birth and smaller in adulthood when born after a brother versus a sister in humans

In mammals, including humans, it is more costly to produce sons than it is to produce daughters, with maternal survival and subsequent reproductive success diminished more by producing male over female offspring. It is therefore predicted that offspring who are produced by mothers who have previously produced sons versus daughters will be compromised by the relatively high cost their mother incurred in the previous reproductive episode. Such effects are potentially important because characters that determine offspring survival and fecundity ultimately contribute to maternal fitness. Using questionnaire-based data from a contemporary human population, I show that birthweight (irrespective of their sex) is lower in individuals born after an elder brother than in those born after an elder sister. In addition, I show that both men and women who were born after a male versus a female sibling have reduced adulthood height, a known correlate of reproductive success in both sexes. The results suggest that producing sons may have a negative effect on the fitness of subsequent offspring, which has implications for calculations of maternal fitness and for optimal sex allocation.     

Early determinants of lifetime reproductive success differ between the sexes in red deer.

In polygynous, sexually dimorphic species, sexual selection should be stronger in males than in females. Although this prediction extends to the effects of early development on fitness, few studies have documented early determinants of lifetime reproductive success in a natural mammal population. In this paper, we describe factors affecting the reproductive success of male and female red deer (Cervus elaphus) on the island of Rum, Scotland. Birthweight was a significant determinant of total lifetime reproductive success in males, with heavier-born males being more successful than lighter ones. In contrast, birthweight did not affect female reproductive success. High population density and cold spring temperatures in the year of birth decreased several components of fitness in females, but did not affect the breeding success of males. The results confirm the prediction that selection on a sexually dimorphic trait should be greater in males than in females, and explain the differential maternal expenditure between sons and daughters observed in red deer. Differences between the sexes in the effects of environmental and phenotypic variation on fitness may generate differences in the amount of heritable genetic variation underlying traits such as birthweight.     

Multiple Mating Increases Fecundity, Fertility and Relative Clutch Mass in the Female Leopard Gecko (Eublepharis macularius)

Females across many taxa may mate with several males or mate more than once with the same male within one reproductive event. Although many researchers have discussed the effects of multiple mating on reproductive success of females, few studies have attempted to disentangle whether the reproductive success of females differs with respect to whether females mate with multiple males or mate more than once with one male. In this study, we hypothesized that female leopard geckos (Eublepharis macularius) increase aspects of their reproductive success, such as fecundity, fertility and relative clutch mass, by mating more than once within one reproductive event, either by mating repeatedly with the same male or multiply mating with different males. We controlled for the potentially confounding variables of mating frequency and mate number by allowing females to mate once with one male, twice with the same male, or twice with two different males. We found that females that mated with more than one male laid more clutches, exhibited increased egg fertility and invested more in clutches relative to females that mated only once with one male, whereas females that mated twice to the same male were intermediate for these variables. Thus, reproductive success is higher among female leopard geckos that mated with more than one male compared to female leopard geckos that mated only once.     

Bateman's Principle in Cooperatively Breeding Vertebrates: The Effects of Non-breeding Alloparents on Variability in Female and Male Reproductive Success

The sex-specific slopes of Bateman's gradients have importantimplications for understanding animal mating systems, includingpatterns of sexual selection and reproductive competition. Intersexualdifferences in the fitness benefits derived from mating withmultiple partners are expected to yield distinct patterns ofreproductive success for males and females, with variance indirect fitness predicted to be greater among males. These analysesassume that typically all adults are reproductive and that failureto produce offspring is non-adaptive. Among some species ofcooperatively breeding birds and mammals, however, non-breedingadult alloparents are common and may comprise the majority ofindividuals in social groups. The presence of a large numberof non-breeding adults, particularly when coupled with greatersocial suppression of reproduction among females, may alterthe relative variance in direct fitness between the sexes, therebygenerating an apparent contradiction to Bateman's Paradigm.To explore quantitatively the effects of non-breeding alloparentson variance in reproductive success, we used genetic estimatesof parentage and reproductive success drawn from the literatureto calculate the relative variability in direct fitness forfemales and males in alloparental and "other" societies of birdsand mammals. Our analyses indicate that in mammals and, to alesser extent, in birds, variability in direct fitness is greateramong females in species characterized by the presence of non-breedingalloparents. These data suggest that social interactions, includingsocial suppression of reproduction, are powerful determinantsof individual direct fitness that may modify sex-specific patternsof reproductive variance from those described by Bateman.     

Female survival,lifetime reproductive success and mating status in a passerine bird

In facultatively polygynous birds, secondary females of polygynously mated males typically have reduced annual reproductive success, because polygynous males provide less paternal care than monogamous males. Life history theory predicts that, as a result of increased reproductive investment, secondary females should suffer from reduced survival and lifetime reproductive success, but previous studies provided only weak support for this hypothesis. We used 7 years of data to study the fitness of female collared flycatchers Ficedula albicollis in relation to mating status by estimating survival and lifetime reproductive success. Taking differences in recapture probability into account, a mark-recapture analysis revealed that females observed at least once to breed as secondary female had higher survival than other females. This relationship was not confounded by laying date, because when we assessed the impact of laying date on survival, we found similar survival patterns. Females of polygynous males had reduced breeding success in terms of number of young fledged during the current reproductive event. However, during their lifetime females found at least once in primary or secondary mating status produced significantly more eggs, and at least the same number of fledglings and recruits as monogamous females. Thus, in the collared flycatcher, females of polygynously mated males seem to suffer from mating status during the most recent reproductive event, but considering survival and lifetime reproductive success, the apparently disadvantageous mating event is not necessarily associated with reduced residual reproductive value.     

Adaptive Offspring Sex Ratio Depends on Male Tail Length in the Guppy

A biased sex ratio in a brood is considered to be an adaptive strategy under certain circumstances. For example, if the expected reproductive success of one sex is greater than that of the other, parents should produce more offspring of the former sex than the latter. A previous study has documented that in the guppy, Poecilia reticulata, the female offspring of males possessing proportionally longer tails exhibit smaller body sizes and show decreased reproductive outputs than those of males having shorter tails. On the other hand, the total lengths of the male offspring of the long‐tailed males are larger because of their longer tails; consequently, they exhibit greater sexual attractiveness to females. Therefore, it has been hypothesized that this asymmetry in the expected reproductive success between the male and female offspring of long‐tailed males may result in a biased sex ratio that is dependent on the tail lengths of their fathers. This hypothesis was tested in the present study. The results showed that the females that mated with long‐tailed males produced more male offspring than those that mated with short‐tailed males. Logistic regression analysis showed that the ratio of tail length to the standard length of the fathers is a determinant factor of the sex of their offspring. These results suggest that the manipulation of the offspring sex ratios by parents enhances the overall fitness of the offspring.     

Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner

Vertebrates have an immature immune system soon after birth, and parasites can therefore be particularly virulent to young hosts. Transfer of immune factors via the egg can give rise to early maternal effects with important consequences for offspring fitness, as maternally derived immunity confers anti-parasite protection. Mothers are expected to allocate immunity differentially to the eggs according to the reproductive value of their offspring as influenced by the quality of their father. In this study, we analysed transmission to the yolk of antibodies specific to an antigen (Newcastle disease virus vaccine, NDV) by vaccinated female barn swallows (Hirundo rustica) mated to males whose secondary sexual characteristics had been manipulated. Concentration of anti-NDV antibodies in the yolk positively covaried with that in maternal plasma. Anti-NDV antibodies were more concentrated in the first but not the fourth eggs laid by females mated with tail-elongated males compared with those mated with tail-shortened and control males. This experiment shows that allocation of maternal immune factors to the eggs is affected by quality of the male, as signalled by its secondary sexual characteristic. Thus, early maternal effects are influenced by sexual attractiveness of male mates and are mediated by immunity.     

Good genes and the maternal effects of polyandry on offspring reproductive success in the bulb mite

Genetic benefits are potentially the most robust explanation of the controversial issue of evolutionary maintenance of polyandry, but the unambiguous demonstration of such benefits has been hindered by the possibility of their confusion with maternal effects. Previous research has shown that polyandrous bulb mite females produce daughters with higher fecundity than monandrous females. Here, we investigate whether this effect arises because polyandrous females invest more in their offspring, or because their offspring inherit 'good genes' from their fathers. Females were mated with either one or four (different) males. However, by sterilizing three of the four males with ionizing radiation, we eliminated any chance of sexual selection (in the polyandrous treatment) so that any differences in the female mating regimes must have been owing to maternal effects. Polyandry had no significant effect on daughter fecundity, thus indicating that any previously documented effects must have been genetic. This was further supported by a significant association between fathers' offensive sperm-competitive ability and the fecundity of their daughters. The association with fathers' sperm defensive ability was not significant, and neither was the association between fathers' sperm competitiveness and sons' reproductive success. However, sons of polyandrous females had lower reproductive success than sons of monandrous females. This shows that the maternal effects of polyandry should be taken into account whenever its costs and benefits are being considered.     

Evolutionary trade-offs of insect resistance to Bacillus thuringiensis crops: fitness cost affecting paternity

Evolution of resistance to insecticides provides a useful model for examining fitness trade-offs associated with adaptation to stress. Here, we examined male reproductive costs in pink bollworm (Pectinophora gossypiella) resistant to an insecticidal protein of Bacillus thuringiensis (Bt) produced by transgenic cotton, using contrasts between two pairs of related susceptible and resistant strains. Without competition for access to females, no costs affecting reproductive success of resistant males were observed. Resistant and susceptible males had similar mating frequency and fertility. Additionally, fecundity of females mated to resistant and susceptible males was comparable. In competition for matings with virgin females, resistant and susceptible males had comparable success in one strain, whereas susceptible males tended to mate more often than resistant males in the other. However, irrespective of strain origin, resistant males that mated first sired significantly less offspring than susceptible males that mated first. The reduced first-male paternity in resistant males may involve reduced sperm precedence caused by mutations in a cadherin gene linked with resistance to Bt cotton.     

The Starling Mating System as an Outcome of the Sexual Conflict

Many bird species demonstrate a variable mating system, with some males being monogamously mated and other males able to attract more than one mate. This variation in avian mating systems is often explained in terms of potential costs of sharing breeding partners and compensation for such costs. However, whenever there is a difference in the optimal mating system for males and females, a sexual conflict over the number of partners is expected. This paper contains a verbal model of how a conflict between male and female European starlings (Sturnus vulgaris),resulting from the fitness consequences of different mating systems for males and females differing over time, determines the mating system. We demonstrate that males and females have contrasting fitness interests regarding mating system, such that males gain from attracting additional mates whereas already mated females pay a cost in terms of reduced reproductive success if males are successful in attracting more mates. We demonstrate how this can be traced to the rules by which males allocate non-sharable care between different broods. Furthermore, we demonstrate that there exist male and female conflict behaviours with the potential to affect the mating system. For example, aggression from already mated females towards prospecting females can limit male mating success and males can circumvent this by spacing the nest-sites they defend. The realised mating system will emerge as a consequence of both the fitness value of the different mating systems for males and females, and the costs for males and females of intersexual competition. We discuss how this model can be developed and critically evaluated in the future.     

Impaired sperm quality,delayed mating but no costs for offspring fitness in crickets winning a fight

The outcome of male–male contest competition is known to affect male mating success and is believed to confer fitness benefits to females through preference for dominant males. However, by mating with contest winners, females can incur significant costs spanning from decreased fecundity to negative effects on offspring. Hence, identifying costs and benefits of male dominance on female fitness is crucial to unravel the potential for a conflict of interests between the sexes. Here, we investigated males' pre‐ and post‐copulatory reproductive investment and its effect on female fitness after a single contest a using the field cricket Gryllus bimaculatus. We allowed males to fight and immediately measured their mating behaviour, sperm quality and offspring viability. We found that males experiencing a fight, independently of the outcome, delayed matings, but their courtship effort was not affected. However, winners produced sperm of lower quality (viability) compared to losers and to males that did not experience fighting. Results suggest a trade‐off in resource allocation between pre‐ and post‐mating episodes of sexual selection. Despite lower ejaculate quality, we found no fitness costs (fecundity and viability of offspring) for females mated to winners. Overall, our findings highlight the importance of considering fighting ability when assessing male reproductive success, as winners may be impaired in their competitiveness at a post‐mating level.     

Polygyny and its fitness consequences for primary and secondary female pied flycatchers

In polygynous species with biparental care, the amount of paternal support often varies considerably. In the pied flycatcher (Ficedula hypoleuca), females mated with monogamous males receive more male assistance during the nestling phase than females mated with bigynous males, as the latter have to share their mates with another female. Bigynous males, however, give more support to their primary broods than to their secondary broods. Using a long-term dataset (31 years), the present study revealed that direct reproductive success, i.e. number of fledglings, was lower in females that mated with bigynous males, especially in secondary broods without male assistance, than in females that mated with monogamous males. Secondary broods with male assistance were more affected than primary broods. Female survival was independent of mating status. In primary broods, a delayed compensation for inferior direct reproductive success was found in terms of the number of grandoffspring, a phenomenon that did not occur in secondary broods. Delayed compensation in primary broods refers to indirect effects, i.e. good genes. According to the sexy son hypothesis, genetically superior (i.e. sexy) males may have sons with a higher number of broods belonging to a polygynous breeding status than do sons from broods with a monogamous father. This was indeed the case for sons descending from primary broods, but not for sons descending from secondary broods.     

Position in the laying order has sex-specific consequences for reproductive success in adult black-headed gulls

Mothers who produce multiple offspring within one reproductive attempt often allocate resources differentially; some maternally derived substances are preferentially allocated to last-produced offspring and others to first-produced offspring. The combined effect of these different allocation regimes on the overall fitness of offspring produced early or late in the sequence is not well understood, partly because production order is often coupled with birth order, making it difficult-to-separate effects of pre-natal maternal allocation from those of post-natal social environments. In addition, very little is known about the influence of laying order on fitness in later life. In this study, we used a semi-natural captive colony of black-headed gulls to test whether an offspring's position in the laying order affected its early-life survival and later-life reproductive success, independent of its hatching order. Later-laid eggs were less likely to hatch, but among those that did, survival to adulthood was greater than that of first-laid eggs. In adulthood, the laying order of females did not affect their likelihood of breeding in the colony, but male offspring hatched from last-laid eggs were significantly less likely to gain a breeding position than earlier-laid males. In contrast, later-laid female parents hatched lower proportions of their clutches than first-laid females, but hatching success was unrelated to the laying order of male parents. Our results indicate that gull mothers induce complex and sex-specific effects on both the early survival of their offspring and on long-term reproductive success through laying order effects among eggs of the same breeding attempt.     

Unpredictable offspring survivorship in the damselfly, Megaloprepus coerulatus, shapes parental behavior, constrains sexual selection, and challenges traditional fitness estimates

Evolutionary biologists typically assume that the number of eggs fertilized or developing embryos produced is correlated with an individual's fitness. Using microsatellite markers, we document for the first time estimates of realized fitness quantified as the number of offspring surviving to adulthood in an insect under field conditions. In a territorial damselfly whose males defend tree hole oviposition sites, patterns of offspring survivorship could not be anticipated by adults. Fewer than half of the parents contributing eggs to a larval habitat realized any reproductive success from their investment. The best fitness correlate was the span over which eggs in a clutch hatched. Among parents, female fecundity and male fertilization success were poor predictors of realized fitness. Although body size was correlated with female clutch size and male mating success, larger parents did not realize greater fitness than smaller ones. The uncoupling of traditional fitness surrogates from realized fitness provides strong empirical evidence that selection at the larval stage constrains selection on mated adults.     

Adaptive female choice for middle-aged mates in a lekking sandfly

Most theoretical models of age-related mate choice predict that females should prefer older males because they have proven survival ability. An alternative view is that older males represent inferior mates because of negative genetic correlations between early and late fitness components, or because older males have traded off longevity against other fitness components, have accumulated deleterious germ-line mutations, or are less well adapted to current conditions than more recently born individuals. While numerous studies have reported female choice for older males, few have explicitly examined the fitness consequences of such a preference. We present evidence from a lekking sandfly, Lutzomyia longipalpis, showing that choosy females discriminate against older males and gain a fitness benefit from their choice. When permitted free choice from an aggregation consisting of males aged zero to two days (young), four to six days (middle-aged) and eight to ten days (old), females preferentially mated with middle-aged males, but all measures of female reproductive success were independent of male age. In contrast, when a second set of females was randomly assigned single virgin males of known age, the eggs of those paired to old mates exhibited lower hatching success than the eggs of females mated to young or middle-aged males. These results suggest that females avoid mating with older males because they represent poorer quality mates. Age-related differences in male quality may have a genetic basis, but could equally well arise through a phenotypic decline in sperm quality or sperm transfer ability with male age. The lack of evidence of female discrimination against older males from other studies may be because these did not explore the reproductive success of the full age range of males.     

Father–offspring phenotypic correlations suggest intralocus sexual conflict for a fitness-linked trait in a wild sexually dimorphic mammal

In sexually dimorphic and polygynous mammals, sexual selection often favours large males with well-developed weaponry, as these secondary sexual characters confer advantages in intrasexual competition and are often preferred by females. Little is known, however, about the effects of sexually selected paternal traits on offspring phenotype in wild mammals, especially when considering that shared phenotypic traits and selection can also differ greatly between genders. Here, we conducted molecular parentage analyses in a long-term study population of mountain goats (Oreamnos americanus), an ungulate exhibiting high sexual dimorphism in mass, to first assess the determinants of yearly reproductive success (YRS) in males. We then examined the effects of paternal characteristics on offspring mass at 1 year of age. Paternity was highly skewed, with 9 per cent of 57 males siring 51 per cent of 96 offspring assigned over 12 years. Male YRS increased with age until apparent reproductive senescence at 9 years, but mass was a stronger determinant of siring success than age, horn length or social rank. Mass of sons increased with paternal mass, but the mass of daughters was negatively related to that of their father, a finding consistent with recent theory on intralocus sexual conflict. Because early differences in mass persisted to early adulthood, sex-specific effects of paternal mass can have important fitness consequences, as adult mass is positively linked with reproduction in both sexes. Divergent father–offspring phenotypic correlations may partly explain the maintenance of sexual dimorphism in mountain goats and the large variance observed for this homologous trait within each gender in polygynous mammals.