Fitness consequences of selfing and outcrossing in the cestode Schistocephalus solidus

Mixed-mating, that is reproduction by both self-fertilizationand cross-fertilization is common in hermaphroditic parasites.Its maintenance poses, however, a problem for evolutionary biology.The tapeworm Schistocephalus solidus Müller 1776, servedas a model to study experimentally the consequences of selfingand outcrossing in its 2 consecutive intermediate hosts, a copepod(Macrocyclops albidus Jurine) and the three-spined sticklebackfish (Gasterosteus aculeatus). Size-matched tapeworms were allowedto reproduce either alone or in pairs in an in vitro systemthat replaced the definitive bird host's gut. Selfed eggs fromsingletons had a 4 times lower hatching success than outcrossedeggs from pairs. Outcrossed offspring achieved both a higherinfection success and a higher weight in the copepod, and ahigher number of parasites per host in both intermediate hosts,but only under competition. Outcrossed offspring were generallymore successful. If a S. solidus plerocercoid has a partnerin the bird's gut, they should outcross unless they differ insize and thus cannot solve the Hermaphrodite's Dilemma cooperatively.Using microsatellite markers, the proportion of selfed offspringand the total reproductive output of each worm within pairsvarying in mean weight and in weight difference was measured.Worms produced more selfed offspring not only with increasingweight difference as expected but also with decreasing totalweight of the pair. If small worms were selfed, they have alreadypurged deleterious mutations and would thus be better selfersin a year with low parasite density when worms cannot find partners.To maintain this advantage they should self a higher proportionof their eggs even with a partner. Here I review recent exprimentalevidence.     

The Hermaphrodite's Dilemma

Given sexual conflict, mating encounters between simultaneous hermaphrodites will conform to a new, conditional, non-zero sum game of strategy, the Hermaphrodite's Dilemma; special cases of which include Prisoner's Dilemma and Game of Chicken. The model predicts that hermaphrodite mating systems will be based on reciprocation with cheating in a preferred sexual role. This model suggests that study of hermaphrodite mating systems will provide direct evidence for the existence of sexual conflict and suggests that sexual conflict may act to stabilize hermaphroditism through such mating systems.     

Social facilitation affects longevity and lifetime reproductive success in a self-fertilizing land snail

Factors that reduce the reproductive output of self-fertilizing hermaphrodites are receiving increasing attention. The combined effects of reduced fecundity of selfing parents and inbreeding depression of the progeny have been referred to as self-fertilization depression. In isolated freshwater snails the reproductive output of selfing individuals also decreases due to the lack of social facilitation (absence of a conspecific). We examined the effect of social facilitation on lifetime reproductive success (number of young produced and longevity) over two generations in the simultaneously hermaphroditic land snail Balea perversa . In a parallel study we showed that B. perversa kept singly and in pairs reproduced exclusively by self-fertilization. In the parent generation, snails kept singly produced less offspring than snails kept in pairs. The difference in lifetime number of young was mainly due to differences in adult life span. Snails of the two groups did not differ in reproductive rate (number of young produced per 100 d of reproductive life) and hatchling size. In the offspring generation, snails kept singly did not differ from individuals kept in pairs in the lifetime number of young and hatchling survival. As in the parent generation, snails kept singly reproduced during a shorter period than snails kept in pairs. However, the shorter reproductive life span of snails kept singly was compensated for by a slightly (but not significantly) higher reproductive rate which resulted in a similar number of offspring produced for both groups. In both generations, snails of the two groups did not differ in size at first reproduction, adult growth rate and size at death. These findings suggest that social facilitation may affect longevity in selfing B. perversa .     

Occurrence,costs and heritability of delayed selfing in a free‐living flatworm

Evolutionary theory predicts that in the absence of outcrossing opportunities, simultaneously hermaphroditic organisms should eventually switch to self‐fertilization as a form of reproductive assurance. Here, we report the existence of facultative self‐fertilization in the free‐living flatworm Macrostomum hystrix, a species in which outcrossing occurs via hypodermic insemination of sperm into the parenchyma of the mating partner. First, we show that isolated individuals significantly delay the onset of reproduction compared with individuals with outcrossing opportunities (‘delayed selfing’) as predicted by theory. Second, consistent with the idea of M. hystrix being a preferential outcrosser under natural conditions, we report likely costs of selfing manifested via reduced hatchling production and offspring survival. Third, we demonstrate that selfing propensity has a genetic basis in this species, with a heritability estimated at 0.43 ± 0.11. Variation in selfing propensity could arise due to differing costs of inbreeding among families; despite marked inter‐family variation in apparent costs of inbreeding, we found no evidence for such a link. Alternatively, selfing propensity might differ across families because of heritable variation in reproductive traits that determine the likelihood of selfing. We speculate that adaptations to hypodermic insemination under outcrossing, most notably a highly modified copulatory stylet (male copulatory organ) and reduced sperm complexity, could also facilitate facultative selfing in this species.     

Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating

Hermaphroditic individuals can produce both selfed and outcrossed progeny, termed mixed mating. General theory predicts that mixed-mating populations should evolve quickly toward high rates of selfing, driven by rapid purging of genetic load and loss of inbreeding depression (ID), but the substantial number of mixed-mating species observed in nature calls this prediction into question. Lower average ID reported for selfing than for outcrossing populations is consistent with purging and suggests that mixed-mating taxa in evolutionary transition will have intermediate ID. We compared the magnitude of ID from published estimates for highly selfing (r > 0.8), mixed-mating (0.2 ≤ r ≥ 0.8), and highly outcrossing (r < 0.2) plant populations across 58 species. We found that mixed-mating and outcrossing taxa have equally high average lifetime ID (δ= 0.58 and 0.54, respectively) and similar ID at each of four life-cycle stages. These results are not consistent with evolution toward selfing in most mixed-mating taxa. We suggest that prevention of purging by selective interference could explain stable mixed mating in many natural populations. We identify critical gaps in the empirical data on ID and outline key approaches to filling them.     

The mixed mating system of the sea palm kelp Postelsia palmaeformis: few costs to selfing

Naturally isolated populations have conflicting selection pressures for successful reproduction and inbreeding avoidance. These species with limited seasonal reproductive opportunities may use selfing as a means of reproductive assurance. We quantified the frequency of selfing and the fitness consequences for inbred versus outcrossed progeny of an annual kelp, the sea palm (Postelsia palmaeformis). Using experimentally established populations and microsatellite markers to assess the extent of selfing in progeny from six founding parents, we found the frequency of selfing was higher than expected in every population, and few fitness costs were detected in selfed offspring. Despite a decline in heterozygosity of 30 per cent in the first generation of selfing, self-fertilization did not affect individual size or reproduction, and correlated only with a marginally significant decline in survival. Our results suggest both that purging of deleterious recessive alleles may have already occurred and that selfing may be key to reproductive assurance in this species with limited dispersal. Postelsia has an alteration of a free-living diploid and haploid stage, where the haploid stage may provide increased efficiency for purging the genetic load. This life history is shared by many seaweeds and may thus be an important component of mating system evolution in the sea.     

BEST OF BOTH WORLDS? ASSOCIATION BETWEEN OUTCROSSING AND PARASITE LOADS IN A SELFING FISH

Mixed-mating strategies (i.e., intermediate levels of self-fertilization and outcrossing in hermaphrodites) are relatively common in plants and animals, but why self-fertilization (selfing) rates vary so much in nature has proved difficult to explain. We tested the hypothesis that parasites help maintain mixed-mating using a partially selfing fish (Kryptolebias marmoratus) as a model. We show that outcrossed progeny in the wild are genetically more diverse and less susceptible to multiple parasite infections than their selfed counterparts. Given that outcrossing in K. marmoratus can only be attained by male-hermaphrodite matings, our data provide an explanation for the coexistence of males and hermaphrodites in androdioecious species where hermaphrodites are unable to outcross among themselves. Moreover, our study provides evidence that parasites contribute to maintaining mixed-mating in a natural animal population.     

Multiple mating in the traumatically inseminating Warehouse pirate bug, Xylocoris flavipes: effects on fecundity and longevity

Optimal mating frequencies differ between sexes as a consequence of the sexual differentiation of reproductive costs per mating, where mating is normally more costly to females than males. In mating systems where sexual reproduction is costly to females, sexual conflict may cause both direct (i.e. by reducing female fecundity or causing mortality) and indirect (i.e. increased risk of mortality, reduced offspring viability) reductions in lifetime reproductive success of females, which have individual and population consequences. We investigated the direct and indirect costs of multiple mating in a traumatically inseminating (TI) predatory Warehouse pirate bug, Xylocoris flavipes (Reuter) (Hemiptera: Anthocoridae), where the male penetrates the female's abdomen during copulation. This study aimed to quantify the effects of TI on female fecundity, egg viability, the lifetime fecundity schedule, longevity and prey consumption in this cosmopolitan biocontrol agent. We found no difference in the total reproductive output between mating treatments in terms of total eggs laid or offspring viability, but there were significant differences found in daily fecundity schedules and adult longevity. In terms of lifetime reproduction, female Warehouse pirate bugs appear to be adapted to compensate for the costs of TI mating to their longevity.     

Mediation of a corticosterone-induced reproductive conflict

Current research in birds suggests that a conflict should exist during reproduction for the role of the glucocorticoid corticosterone (CORT). While elevated levels have been correlated with the increased energetic demand of raising offspring, elevated CORT levels have traditionally been implicated in reproductive abandonment. We examined the relationship between CORT and nest desertion in breeding wild female European starlings (Sturnus vulgaris) incorporating analyses of both total circulating levels and 'free', unbound CORT through analysis of corticosteroid-binding globulin (CBG). Free baseline CORT levels of nest-abandoning birds were significantly higher than nonabandoning birds within each stage, with chick-rearing birds exhibiting the highest free baseline CORT levels, while concurrently remaining the most resistant stage to nest desertion. Elevated free baseline CORT levels in chick-rearing birds were not due to increased total CORT secretion, but rather to a decrease in CBG levels. Overall, our results suggest that CORT and CBG interact to play a role in mediating the increased energetic demand of offspring, while minimizing the chances of nest desertion, thereby alleviating any potential behavioral conflict for CORT during reproduction. Furthermore, these results demonstrate that the traditional view of the role of CORT during reproduction is much more complex than previously appreciated. Together with mounting evidence, we suggest that elevated corticosteroid levels are an inherent and necessary part of reproduction in nonmammalian tetrapods.     

Reproductive system of a mixed-mating plant responds to climate perturbation by increased selfing

How plants respond to climatic perturbations, which are forecasted to increase in frequency and intensity, is difficult to predict because of the buffering effects of plasticity. Compensatory adjustments may maintain fecundity and recruitment, or delay negative changes that are inevitable but not immediately evident. We imposed a climate perturbation of warming and drought on a mixed-mating perennial violet, testing for adjustments in growth, reproduction and mortality. We observed several plasticity-based buffering responses, such that the climatic perturbation did not alter population structure. The most substantial reproductive adjustments, however, involved selfing, with a 45% increase in self-pollination by chasmogamous flowers, a 61% increase in the number of cleistogamous flowers that produced at least one fruit and an overall 15% increase in fruit production from selfed cleistogamous flowers. Reproductive assurance thus compensated for environmental change, including low pollinator visitation that occurred independently of our climate treatment. There was also no immediate evidence for inbreeding depression. Our work indicates that plants with vegetative and reproductive flexibility may not be immediately and negatively affected by a climatic perturbation. The stabilizing effects of these reproductive responses in the long term, however, may depend on the implications of significantly elevated levels of selfing.     

Allee effect and self-fertilization in hermaphrodites: reproductive assurance in a structured metapopulation

Reproductive assurance through selfing during colonization events or when population densities are low has often been put forward as a mechanism selecting for the evolution of self-fertilization. Such arguments emphasize on the role of both local demography and metapopulation processes. We developed a model for the evolution of self-fertilization in a structured metapopulation in which local densities are not steady because of population growth. Reproduction by selfing is density-independent (reproductive assurance) but selfed seeds endure inbreeding depression, whereas reproduction by outcrossing is density-dependent (Allee effect). First, we derived an analytical criterion for metapopulation viability as a function of the selfing rate and metapopulation parameters. We show that outcrossers can develop a viable metapopulation when they produce a high amount of dispersal seeds that counterbalances their incapacity to found new populations from low densities. Second, the model shows there is a positive feedback between demography and outcrossing rates, leading to either complete outcrossing or selfing. Specifically, we illustrate that inbreeding depression can paradoxically favor the evolution of selfing because of its negative effect on density. Also, complete outcrossing can be selected despite pollen limitation, although it does not provide a full seed set. This model underlines the influence of the mating system both on demography and gene dynamics in a metapopulation context.     

Combined effects of bottlenecks and selfing in populations of Corella eumyota, a recently introduced sea squirt in the English Channel

The success of an exotic species depends notably on its capacity to initiate a new population from a few individuals, to survive genetic bottlenecks and to adapt locally. Species with multiple reproductive strategies (e.g. mixed-mating system with both self- and cross-fertilization) can be efficient colonizers. Herein we focus on Corella eumyota , an exotic ascidian that has rapidly invaded English Channel coasts in recent years. Interestingly, this brooding hermaphroditic ascidian is capable of self-fertilization in the laboratory. We developed 12 microsatellite markers from an enriched library of genomic DNA to investigate the level of inbreeding and selfing in two putatively native populations (South Africa, N  = 34, and New Zealand, N  = 28) and to examine if founder effects were possibly associated with its recent introduction in two French populations (Perros-Guirec, N  = 22 and Brest; N  = 25). Genetic polymorphism was very low in both native populations (i.e. less than 60% of the loci were polymorphic) and even lower in the introduced populations, one of which was monomorphic at all loci, suggesting a recent bottleneck. F _is and a new method based on multi-locus heterozygosity were used to provide estimates of inbreeding. A high selfing rate was inferred in the South Africa population with both methods ( s  = 0.90), whereas in the other native population (New Zealand) a lower but significant estimate of selfing rate ( s  = 0.29) was obtained with the multi-locus method. This variability of population selfing rate might be explained by a mixed-mating system, allowing C. eumyota to reproduce through inbreeding and outbreeding according to mating possibilities; this trait may have favoured the rapid establishment of new populations in Europe.     

Oxidative shielding and the cost of reproduction

Life‐history theory assumes that reproduction and lifespan are constrained by trade‐offs which prevent their simultaneous increase. Recently, there has been considerable interest in the possibility that this cost of reproduction is mediated by oxidative stress. However, empirical tests of this theory have yielded equivocal support. We carried out a meta‐analysis to examine associations between reproduction and oxidative damage across markers and tissues. We show that oxidative damage is positively associated with reproductive effort across females of various species. Yet paradoxically, categorical comparisons of breeders versus non‐breeders reveal that transition to the reproductive state is associated with a step‐change reduction in oxidative damage in certain tissues and markers. Developing offspring may be particularly sensitive to harm caused by oxidative damage in mothers. Therefore, such reductions could potentially function to shield reproducing mothers, gametes and developing offspring from oxidative insults that inevitably increase as a consequence of reproductive effort. According to this perspective, we hypothesise that the cost of reproduction is mediated by dual impacts of maternally‐derived oxidative damage on mothers and offspring, and that mothers may be selected to diminish such damage. Such oxidative shielding may explain why many existing studies have concluded that reproduction has little or no oxidative cost. Future advance in life‐history theory therefore needs to take account of potential transgenerational impacts of the mechanisms underlying life‐history trade‐offs.     

Maternal effects on offspring size in a natural population of the viviparous tsetse fly

1. Theory predicts that mothers should adaptively adjust reproductive investment depending on current reserves and future reproductive opportunities. Females in better intrinsic state, or with more resources, should invest more in current reproduction than those with fewer resources. Across the lifespan, investment may increase as future reproductive opportunities decline, yet may also decline with reductions in intrinsic state. 2. Across many species, larger mothers produce larger offspring, but there is no theoretical consensus on why this is so. This pattern may be driven by variation in maternal state such as nutrition, yet few studies measure both size and nutritional state or attempt to tease apart confounding effects of size and age. 3. Viviparous tsetse flies (Glossina species) offer an excellent system to explore patterns of reproductive investment: females produce large, single offspring sequentially over the course of their relatively long life. Thus, per‐brood reproductive effort can be quantified by offspring size. 4. While most tsetse reproduction research has been conducted on laboratory colonies, maternal investment was investigated in this study using a unique field method where mothers were collected as they deposited larvae, allowing simultaneous mother‐offspring measurements under natural conditions. 5. It was found that larger mothers and those with a higher fat content produced larger offspring, and there was a trend for older mothers to produce slightly larger offspring. 6. The present results highlight the importance of measuring maternal nutritional state, rather than size alone, when considering maternal investment in offspring. Implications for understanding vector population dynamics are also discussed.     

Asynchrony between solitary bee emergence and flower availability reduces flower visitation rate and may affect offspring size

Climate change can disrupt plant-pollinator interactions when shifts in the timing of pollinator activity and flowering occur unequally (i.e., phenological asynchrony). Phenological asynchrony between spring-emerging solitary bees and spring-flowering plants may cause bees to experience food deprivation that can affect their reproductive success. However, the mechanisms underlying the effects of food deprivation on solitary bee reproduction remain unknown. We investigated 1) whether food deprivation caused by phenological asynchrony affects solitary bee reproduction by influencing female lifespan and/or visitation to flowers, and 2) the relationship between the magnitude of asynchrony and bee responses. We simulated phenological asynchrony by depriving emerged female Osmia cornifrons (a spring-active solitary bee species) of nectar and pollen for 0 to 16 days. Following asynchrony treatments, we used flight cages to monitor 1) post-treatment female lifespan, 2) flower visitation, and 3) reproduction (i.e., total offspring, offspring weight, sex ratio). We found that post-treatment female lifespan was not affected by phenological asynchrony treatments, but that flower visitation rate and offspring weight decreased as the magnitude of asynchrony increased. Due to low offspring production and a lack of female offspring across treatments, we were unable to assess the effects of phenological asynchrony on total offspring produced or sex ratio. Findings suggest that post-emergence food deprivation caused by phenological asynchrony may affect offspring size by influencing nest-provisioning rates. In solitary bees, body size influences wintering survival, fecundity, and mating success. Thus, phenological asynchrony may have consequences for solitary bee populations that stem from reduced flower visitation rates, and these consequences may increase as the magnitude of asynchrony increases. Because many wild flowering plants and crops rely on pollination services provided by bees for reproductive success, bee responses to phenological asynchrony may also affect wild plant biodiversity and crop yields.     

Fitness consequences of divorce in the azure-winged magpie depends on the breeding experience of a new mate

Sexual conflict in producing and raising offspring is a critical issue in evolutionary ecology research.Individual experience affects their breeding performance,as measured by such traits of provisioning of offspring and engagement in extra-pair copulations,and may cause an imbalance in sexual conflict.Thus,divorce is hypothesized to occur within aged social pairs,irrespective of current reproductive success.This concept was explored in the azure-winged magpie Cyanopica cyanus by investigating the divorce of a social pair and its relationship to their changes in breeding performance with prior experience.Females engaging in extra-pair copulation may intensify sexual conflicts and may be the main reason for divorce.Once divorced,females repairing with an inexperienced male realized higher reproductive success than that repairing with an experienced male;males repairing with an experienced female realized higher reproductive success than that repairing with an inexperienced female.This finding indicates that the fitness consequence of divorce depends on the breeding experience of new mates.Divorced females can obtain more extra-pair copulations,whereas divorced males cannot,when they repair with inexperienced breeders.Divorced females provisioned a brood at lower rates than inexperienced females whereas divorced males had no such difference.It appears that divorced females can obtain an advantage in sexual conflicts with inexperienced mates in future reproduction.Consequently,females are probably more active than males in divorcing their aged mates so as to select an inexperienced male as a new mate.Azure-winged magpies thus provide novel insights into the implicaticns of sexual conflict in birds.     

A Prisoner's Dilemma model of the evolution of paternal care

The heavy energetic demands of gestation, lactation and rearing of offspring mean that studies of paternal care in primates usually focus on female reproductive effort. Here it is shown that both male and female reproductive effort must be considered in order to understand how paternal care evolved. This is done using the Prisoner's Dilemma, best known as a model of reciprocal altruism. It is found that the relative cost of reproduction for males and females is crucially important in determining co-operative and competitive strategies. In particular, when male reproductive costs are less than female reproductive costs, males co-operate with females even when females do not reciprocate. This surprising behaviour, termed non-reciprocal altruism, is comparable with male investment in a female and her offspring.     

Effect of mother's physical condition during pregnancy and lactation on postnatal growth and reproductive success of offspring in water vole Arvicola terrestris L

Postnatal growth, life span, and probability of reproduction in the adult state depended on the mother's physical condition during pregnancy and lactation in water vole. The white fat weight in the female abdominal cavity was shown to significantly increase in pregnancy and to decrease in late lactation. As an indicators for nutritional state of females, their body weight difference after parturition (or in late lactation) and expected from the regression equation relating individual body weight at the beginning and the end of each reproductive stage were used (physical condition indexes in pregnancy or lactation). The correlation of the physical condition index in pregnancy with the storage fat weight was 0.67. The metabolic resources of the mother's body proved to favor faster offspring development. The female offspring weight at the age of 3 and 10 weeks as well as adult ones positively correlated with the mother's nutritional state in pregnancy, while the male offspring weight demonstrated a similar correlation at the age of 3 and 6 weeks. Increased negative energy balance during lactation proved to decrease the offspring weight in both sexes after separation from mother and at the age of 6 weeks. High nutritional state of mother in pregnancy favored both the probability of reproduction and life span of female offspring. The reproduction of male offspring did not depend on the mother's physical condition. The life span peaked in male offspring of mothers in a nutritional state below average in pregnancy and above average in lactation. Thus, the physical condition of the mother's body is an important sex-dependent factor of phenotypic variation in the offspring body weight, reproductive competence, and life span.     

The cost of dominance: suppressing subordinate reproduction affects the reproductive success of dominant female banded mongooses

Social species show considerable variation in the extent to which dominant females suppress subordinate reproduction. Much of this variation may be influenced by the cost of active suppression to dominants, who may be selected to balance the need to maximize the resources available for their own offspring against the costs of interfering with subordinate reproduction. To date, the cost of reproductive suppression has received little attention, despite its potential to influence the outcome of conflict over the distribution of reproduction in social species. Here, we investigate possible costs of reproductive suppression in banded mongooses, where dominant females evict subordinates from their groups, thereby inducing subordinate abortion. We show that evicting subordinate females is associated with substantial costs to dominant females: pups born to females who evicted subordinates while pregnant were lighter than those born after undisturbed gestations; pups whose dependent period was disrupted by an eviction attained a lower weight at independence; and the proportion of a litter that survived to independence was reduced if there was an eviction during the dependent period. To our knowledge, this is the first empirical study indicating a possible cost to dominants in attempting to suppress subordinate breeding, and we argue that much of the variation in reproductive skew both within and between social species may be influenced by adaptive variation in the effort invested in suppression by dominants.     

Effect of mother’s physical condition during pregnancy and lactation on postnatal growth and reproductive success of offspring in water vole <Emphasis Type="Italic">Arvicola terrestris</Emphasis>

Postnatal growth, life span, and probability of reproduction in the adult state depended on the mother’s physical condition during pregnancy and lactation in water vole. The white fat weight in the female abdominal cavity was shown to significantly increase in pregnancy and to decrease in late lactation. As an indicators for nutritional state of females, their body weight difference after parturition (or in late lactation) and expected from the regression equation relating individual body weight at the beginning and the end of each reproductive stage were used (physical condition indexes in pregnancy or lactation). The correlation of the physical condition index in pregnancy with the storage fat weight was 0.67. The metabolic resources of the mother’s body proved to favor faster offspring development. The female offspring weight at the age of 3 and 10 weeks as well as adult ones positively correlated with the mother’s nutritional state in pregnancy, while the male offspring weight demonstrated a similar correlation at the age of 3 and 6 weeks. Increased negative energy balance during lactation proved to decrease the offspring weight in both sexes after separation from mother and at the age of 6 weeks. High nutritional state of mother in pregnancy favored both the probability of reproduction and life span of female offspring. The reproduction of male offspring did not depend on the mother’s physical condition. The life span peaked in male offspring of mothers in a nutritional state below average in pregnancy and above average in lactation. Thus, the physical condition of the mother’s body is an important sex-dependent factor of phenotypic variation in the offspring body weight, reproductive competence, and life span.