Complex environmental effects on the expression of alternative reproductive phenotypes in the bulb mite

Understanding the evolution and maintenance of within-sex reproductive morphs, or alternative reproductive phenotypes (ARPs), requires in depth understanding of the proximate mechanisms that determine ARP expression. Most species express ARPs in complex ecological environments, yet little is know about how different environmental variables collectively affect ARP expression. Here, I investigated the influence of maternal and developmental nutrition and sire phenotype on ARP expression in bulb mites (Rhizoglyphus robini), where males are either fighters, able to kill other mites, or benign scramblers. In a factorial experiment, females were raised on a rich or a poor diet, and after maturation they were paired to a fighter or a scrambler. Their offspring were put on the rich or poor diet. Females on the rich diet increased investment into eggs when mated to a fighter, but suffered reduced longevity. Females indirectly affected offspring ARP expression as larger eggs developed into larger final instars, which were more likely to develop into a fighter. Final instar size, which also strongly depended on offspring nutrition, was the main cue for morph development: a switch point, or size threshold, existed where development switched from one phenotype to the other. Sire phenotype affected offspring phenotype, but only if offspring were on the poor diet, indicating a gene by environment interaction. Overall, the results revealed that complex environmental effects can underlie ARP expression, with differential maternal investment potentially amplifying genetic effects on offspring morphology. These effects can therefore play an important role in understanding how selection affects ARP expression and, like quantitative genetics models for continuous traits, should be incorporated into models of threshold traits.     

Paternal indirect genetic effects on offspring viability and the benefits of polyandry

Although females are expected to maximize their reproductive success with only one or a few matings, the females of many species mate with multiple partners. Experimental studies have found evidence for an increase in egg or embryo viability when females mate polyandrously. These studies have been interpreted in the context of genetic-benefit models that propose that multiple mating increases offspring viability because it allows females to select male genotypes that influence viability directly or because it allows females to avoid genetic incompatibility. However, no studies have examined directly the precise mechanisms by which parents influence embryo viability. Using a morphological marker that enabled us to determine paternity and survival of embryos sired by individual male crickets in both sperm-competitive and -noncompetitive situations, we show that males inducing high embryo viability enhance the viability of embryos sired by inferior males. These results indicate that paternal effects and interacting phenotypes determine embryo viability. They show that a male's reproductive success is modified by the interaction between indirect genetic effects of sperm competitors. Importantly, our findings show that the benefits accruing to offspring of multiply mated females need not be transmitted genetically.     

Heritability of sperm competition success in the bulb mite,Rhizoglyphus robini

Multiple mating by females has been proposed to function as a form of mate-choice, which implies that males should show heritable variation in sperm-competitive abilities. In this study, repeatability and heritability of sperm competition success was estimated in the bulb mite, Rhizoglyphus robini. Fertilization success of males was estimated in competition with sperm of two other males. Males differed consistently in their sperm competition success, with repeatability estimated at 0.22. The heritability of sperm competition success was estimated using parent-offspring regression, with the mean fertilization success from two matings used as a measure of each male's competitive ability. There was a significant association between the sperm competition success of fathers and sons. Narrow sense heritability (h²) was 0.284. This result supports the hypotheses proposing the multiple mating is selectively maintained in females by enhancing the reproductive success of their progeny.     

Experimental observations on maternal reproductive rate and offspring characteristics

Starting from a clone of Philodina roseola (Rotifera, Bdelloidea) six homogeneous animals have been reared. From them three different age cohorts have been studied in order to determine their life tables. Cohorts and parental life schedules are compared and discussed. A sort of correlation between offspring fecundity and life span and maternal rate of egg production could be established.     

Effect of inbreeding and heritability of sperm competition success in the bulb mite Rhizoglyphus robini

Sperm competition is a potent evolutionary force shaping the reproductive biology of most animal species. Here, we estimated the heritability of sperm competition success in the promiscuous bulb mite Rhizoglyphus robini. Sperm competition success was measured with the sterile male technique as the proportion of eggs fertilised by the second of three males mated with a single female. Sperm competition success responded significantly to selection. The heritability estimated from the response to five generations of selection was 0.13. We also estimated the effect of inbreeding on sperm competition success. Males produced by sib-mating (F=0.25) had a significantly lower sperm competition success than outbred males. The estimated coefficient of inbreeding depression was 0.53. Such high inbreeding depression together with moderately low heritability is consistent with the view that sperm competitive ability is under strong directional selection and strongly influences the reproductive success of males.     

Role of maternal smoking and maternal reproductive history in the etiology of hypospadias in the offspring

BACKGROUND: This study was undertaken to evaluate some possible risk factors for hypospadias with special regard to parity, subfertility and maternal smoking. METHODS: With the use of the Swedish health registries, 3,262 infants with a diagnosis of hypospadias were identified among 1,413,811 infants born in 1983-96 with prospectively collected smoking exposure during pregnancy. Odds ratios (OR) and 95% confidence intervals (CI) were calculated after adjustment for various possible confounders. RESULTS: A negative association between hypospadias and maternal smoking was found (OR: 0.83 95% CI: 0.76-0.90), but this association was only observed among mothers of Parity 1 or 4+, and the possibility of the results being due to confounding was suspected. Primiparity (vs. Parity 2) was positively associated with hypospadias (OR: 1.29 95% CI: 1.19-1.40), and so was subfertility (defined here as at least 1 year of attempts to conceive) (OR for subfertility: 1.16 95% CI: 1.01-1.33). The OR for smoking and primiparity, respectively, were of the same magnitude irrespective of whether subfertility was present or not, and no evidence was found that subfertility in the parents of infants with hypospadias seriously confounded the analyses. CONCLUSIONS: No explanation was found for the negative association between maternal smoking and hypospadias or the positive association between primiparity and hypospadias. Possible causal mechanisms are discussed.     

The influence of maternal effects on indirect benefits associated with polyandry

Despite numerous and diverse theoretical models for the indirect benefits of polyandry, empirical support is mixed. One reason for the difficulty in detecting indirect benefits of polyandry may be that these are subtle and are mediated by environmental effects, such as maternal effects. Maternal effects may be especially important if females allocate resources to their offspring depending on the characteristics of their mating partners. We test this hypothesis in the burying beetle Nicrophorus vespilloides, a species that provides extensive and direct parental care to offspring. We used a fully factorial design and mated females to one, two, three, four or five different males and manipulated conditions so that their offspring received reduced (12 h) or full (ca 72 h) maternal care. We found that average offspring fitness increased with full maternal care but there was no significant effect of polyandry or the interaction between the duration of maternal care and the level of polyandry on offspring fitness. Thus, although polyandry could provide a mechanism for biasing paternity towards high quality or compatible males, and variation in parental care matters, we found no evidence that female N. vespilloides gain indirect benefits by using parental care to bias the allocation of resources under different mating conditions.     

Infanticide in the evolution of reproductive synchrony: effects on reproductive success

Synchronous breeding in animals and plants has stimulated both a theoretical and empirical examination of the possible benefits of active synchronization. The selective pressures of predation and infanticide are the strongest candidates proposed to explain the evolution of reproductive synchrony. Alternatively, breeding asynchronously with conspecifics may ensure a greater availability of resources per breeder. However, the possible fitness benefits resulting from active asynchronization have not yet received attention in evolutionary ecology. Here we present a hypothesis, based on a graphical model, illustrating the costs and benefits of the two modes of reproduction. We tested the hypothesis empirically using a 2 x 2 full factorial study design, where reproductive synchrony and infanticide tactics were manipulated in enclosed populations of the bank vole. The results reveal a relationship between infanticide tactics and breeding synchrony as illustrated by our hypothesis. In general, female reproductive success (number and size of offspring surviving to weaning) was significantly lower in infanticidal populations. Moreover, an asynchronous breeding pattern proved to be advantageous in the noninfanticidal population but this advantage of asynchrony was lost as infanticide became common in the population. Our findings support the idea that synchronous reproduction could have evolved as a counterstrategy against infanticide.     

Nest-site preference and maternal effects on offspring growth

Maternal preferences for oviposition sites are assumed to beadaptive, but offspring fitness is not always higher at preferredsites and, thus, further study of the selection pressures thatinfluence oviposition behavior is warranted. Among birds, predationis regarded as the primary agent of selection on nest-site microhabitatpreferences, but alternatives are rarely considered. We testedthe hypothesis that avian nest-site preferences are an adaptiveresponse to fitness costs imposed by variation in nest-sitemicroclimate. We documented that Chestnut-collared Longspurs(Calcarius ornatus) strongly preferred to orient nests towardsthe southeast and showed that this preference influenced microclimate:nests facing southeast had the highest midday temperatures.Yet, preferences were not adaptive because nestlings in nestswith the preferred orientation gained mass at a slower rate,had retarded skeletal growth, and reached a smaller final size.We experimentally tested this result by altering orientationof nests and confirmed, for the first time, that variation innestling growth was causally linked to variation in nest microclimatearising from nest-orientation preferences. Adults respondedto the high temperatures at preferred southeast-facing nestsby spending more time shading young from the sun, apparentlyattempting to ameliorate heat costs. This response, however,resulted in parents spending less time feeding young, potentiallyexplaining slower growth in these nests. Direct effects of highertemperatures may also play a role in slower growth. Althoughwe lack an explanation for this apparently maladaptive preference,these results demonstrate that nest-site choices of birds canyield fitness costs imposed by variation in nest microclimate.     

Female polyandry affects their sons’ reproductive success in the red flour beetle Tribolium castaneum

A potential benefit to females mating with multiple males is the increased probability that their sons will inherit traits enhancing their pre‐ or post‐mating ability to obtain fertilizations. We allowed red flour beetle (Tribolium castaneum) females to mate on three consecutive days either repeatedly to the same male or to three different males. This procedure was carried out in 20 replicate lines, 10 established with wild‐type, and 10 with the Chicago black morph, a partially dominant phenotypic marker. The paternity achieved by the sons of females from polyandrous vs. monandrous lines of contrasting morph was assessed in the F1, F2 and F3 generation by mating wild‐type stock females to two experimental males and assigning the progeny to either sire based on phenotype. The sons of polyandrous wild‐type females achieved significantly higher paternity when mating in the second male role than the sons of monandrous wild‐type females. By contrast, when mating in the first male role, males produced by females from polyandrous lines tended to have lower paternity than males from monandrous lines. Both effects were independent of the number of mates of the black competitor’s mother, and interacted significantly with the number of progeny laid by the female. These results provide the first evidence that manipulating the number of mates of a female can influence her sons’ mating success and suggest a potential trade‐off between offence and defence in this species.     

Some effects of mastectomy on reproductive success in the guinea-pig

Virgin guinea-pigs were mastectomized in two stages between 11 and 18 weeks of age and then mated, starting 19 weeks after final surgery. In the subsequent first pregnancy, the incidence of still-births and neonatal deaths was significantly higher in the mastectomized animals (6 out of 12 mothers (50%) and 14 out of 49 young (29%) compared with intact guinea-pigs (1 out of 15 mothers (7%) and 1 out of 58 young (2%)). There was no significant effect of mastectomy on litter size and weight or on gestation period. The still-born were not significantly different in weight from those born alive. A significant relation was found between maternal weight changes in the period 20 to 5 days before parturition and the occurrence of still-births and neonatal deaths; still-births were associated with a period of reduced weight gain. No effect of mastectomy on the length of the oestrous cycle was apparent but a significant increase in the incidence of non-pregnancy was found. The results provide further evidence that mastectomy influences reproductive success in the guinea-pig and suggest that parturition is a key process affected.     

Hormonal manipulation of offspring number: maternal effort and reproductive costs

We used exogenous gonadotropin hormones to physiologically enlarge litter size in the bank vole (Clethrionomys glareolus). This method allowed the study design to include possible production costs of reproduction and a trade-off between offspring number and body size at birth. Furthermore, progeny rearing and survival and postpartum survival of the females took place in outdoor enclosures to capture salient naturalistic effects that might be present during the fall and early winter. The aim of the study was to assess the effects of the manipulation on the growth and survival of the offspring and on the reproductive effort, survival, and future fecundity of the mothers. Mean offspring body size was smaller in enlarged litters compared to control litters at weaning, but the differences disappeared by the winter. Differences in litter sizes disappeared before weaning age due to higher mortality in enlarged litters. In addition to the effects of the litter size, offspring performance was probably also influenced by the ability of the mother to support the litter. Experimental females had higher reproductive effort at birth, and they also tended to have higher mortality during nursing. Combined effects of high reproductive effort at birth and high investment in nursing the litter entailed costs for the experimental females in terms of decreased probability of producing a second litter and a decreased body mass gain. Thus, enlarged litter size had both survival and fecundity costs for the mothers. Our results suggest that the evolution of litter size and reproductive effort is determined by reproductive costs for the mothers as well as by a trade-off between offspring number and quality.     

Producing sons reduces lifetime reproductive success of subsequent offspring in pre-industrial Finns

Life-history theory states that reproductive events confer costs upon mothers. Many studies have shown that reproduction causes a decline in maternal condition, survival or success in subsequent reproductive events. However, little attention has been given to the prospect of reproductive costs being passed onto subsequent offspring, despite the fact that parental fitness is a function of the reproductive success of progeny. Here we use pedigree data from a pre-industrial human population to compare offspring life-history traits and lifetime reproductive success (LRS) according to the cost incurred by each individual's mother in the previous reproductive event. Because producing a son versus a daughter has been associated with greater maternal reproductive cost, we hypothesize that individuals born to mothers who previously produced sons will display compromised survival and/or LRS, when compared with those produced following daughters. Controlling for confounding factors such as socio-economic status and ecological conditions, we show that those offspring born after elder brothers have similar survival but lower LRS compared with those born after elder sisters. Our results demonstrate a maternal cost of reproduction manifested in reduced LRS of subsequent offspring. To our knowledge, this is the first time such a long-term intergenerational cost has been shown in a mammal species.     

Maternal developmental stress reduces reproductive success of female offspring in zebra finches

Environmental factors play a key role in the expression of phenotypic traits and life-history decisions, specifically when they act during early development. In birds, brood size is a main environmental factor affecting development. Experimental manipulation of brood sizes can result in reduced offspring condition, indicating that developmental deficits in enlarged broods have consequences within the affected generation. Yet, it is unclear whether stress during early development can have fitness consequences projecting into the next generation. To study such trans-generational fitness effects, we bred female zebra finches, Taeniopygia guttata, whose mothers had been raised in different experimental brood sizes. We found that adult females were increasingly smaller with increasing experimental brood size in which their mother had been raised. Furthermore, reproductive success at hatching and fledging covaried negatively with the experimental brood size in which their mothers were raised. These results illustrate that early developmental stress can have long-lasting effects affecting reproductive success of future generations. Such trans-generational effects can be life-history responses adapted to environmental conditions experienced early in life.     

Free mutual mate preferences in house mice affect reproductive success and offspring performance

When social constraints on the expression of mate preferences are absent, variation in offspring viability is predicted to favour females and males that display mate preferences. Earlier studies showed that female and male house mice, Mus domesticus, tested individually and mated with preferred (P) partners had higher reproductive success and better progeny performance than individuals mated with nonpreferred (NP) partners. Here we tested the effects of mutual mate preferences on reproductive success, offspring viability and performance. We conducted mate preference tests and created four types of reproductive pairings. One involved females and males that preferred each other (P-P); the second type had females that preferred the male but the male did not prefer the female (P-NP); the third had females that did not prefer the male but the male did prefer the female (NP-P). The last set consisted of females and males that did not prefer each other (NP-NP). We measured components of fitness for breeders (reproductive success) and offspring viability (birth-to-weaning viability and weight variation) as well as measures of offspring performance. There were no statistical differences in reproductive success of breeders or offspring viability and quality (weight variation) among the four types of pairings. There were, however, consistent differences between P-P versus NP-NP matings. The number of pups weaned, time to first litter, birth-to-weaning viability, pup body weight at birth and weaning, and the growth rates for pups of both sexes were consistently greater for progeny from P-P matings than NP-NP matings. Significant differences occurred among the four mating types in dominance of sons during aggression trials, nest construction and predator avoidance. Progeny from P-P matings displayed behaviour associated with higher fitness more often than progeny from NP-NP matings. These data show that breeders produce more highly competent progeny, most likely to survive, when social constraints on the expression of mate preferences in both sexes are relaxed.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.