Evidence for inbreeding depression in a species with limited opportunity for maternal effects

It is often assumed that mating with close relatives reduces offspring fitness. In such cases, reduced offspring fitness may arise from inbreeding depression (i.e., genetic effects of elevated homozygosity) or from post‐mating maternal investment. This can be due to a reduction in female investment after mating with genetically incompatible males (“differential allocation”) or compensation for incompatibility (“reproductive compensation”). Here, we looked at the effects of mating with relatives on offspring fitness in mosquitofish, Gambusia holbrooki. In this species, females are assumed to be nonplacental and to allocate resources to eggs before fertilization, limiting differential allocation. We looked at the effects of mating with a brother or with an unrelated male on brood size, offspring size, gestation period, and early offspring growth. Mating with a relative reduced the number of offspring at birth, but there was no difference in the likelihood of breeding, gestation time, nor in the size or growth of these offspring. We suggest that due to limited potential for maternal effects to influence these traits that any reduction in offspring fitness, or lack thereof, can be explained by inbreeding depression rather than by maternal effects. We highlight the importance of considering the potential role of maternal effects when studying inbreeding depression and encourage further studies in other Poeciliid species with different degrees of placentation to test whether maternal effects mask or amplify any genetic effects of mating with relatives.     

Effects of variation in resource acquisition during different stages of the life cycle on life‐history traits and trade‐offs in a burying beetle

Individual variation in resource acquisition should have consequences for life‐history traits and trade‐offs between them because such variation determines how many resources can be allocated to different life‐history functions, such as growth, survival and reproduction. Since resource acquisition can vary across an individual's life cycle, the consequences for life‐history traits and trade‐offs may depend on when during the life cycle resources are limited. We tested for differential and/or interactive effects of variation in resource acquisition in the burying beetle Nicrophorus vespilloides. We designed an experiment in which individuals acquired high or low amounts of resources across three stages of the life cycle: larval development, prior to breeding and the onset of breeding in a fully crossed design. Resource acquisition during larval development and prior to breeding affected egg size and offspring survival, respectively. Meanwhile, resource acquisition at the onset of breeding affected size and number of both eggs and offspring. In addition, there were interactive effects between resource acquisition at different stages on egg size and offspring survival. However, only when females acquired few resources at the onset of breeding was there evidence for a trade‐off between offspring size and number. Our results demonstrate that individual variation in resource acquisition during different stages of the life cycle has important consequences for life‐history traits but limited effects on trade‐offs. This suggests that in species that acquire a fixed‐sized resource at the onset of breeding, the size of this resource has larger effects on life‐history trade‐offs than resources acquired at earlier stages.     

Unravelling the effects of differential maternal allocation and male genetic quality on offspring viability in the dung beetle, Onthophagus sagittarius

Good genes models of mate choice assume heritability of fitness-related traits. However, maternal effects can inflate estimates of trait heritability, and genotype-environment interactions can have significant effects on good genes processes of evolution. Thus, partitioning genetic and maternal/environmental sources of variation in studies of good genes mate choice represents an empirical challenge. In this study, we used the dung beetle Onthophagus sagittarius to examine additive genetic and maternal effects on egg-to-adult offspring viability. We used a half-sib full-sib breeding design and manipulated the maternally provided environment by reducing or increasing the mass of the brood ball within which each offspring developed. We found evidence of differential allocation of investment by females in the brood balls they produced. However, experimental manipulations of maternal allocation to brood balls had only a weak and non-significant influence on the sire effects on offspring viability. Significant additive genetic effects on offspring viability were pervasive across our manipulations of the maternally provided larval environment. This finding indicates that although females do show differential allocation to offspring based on sire phenotype, ‘good genes’ benefits of mate choice are not dependent upon differential maternal allocation.     

Links between parental life histories of wild salmon and the telomere lengths of their offspring

The importance of parental contributions to offspring development and subsequent performance is self‐evident at a genomic level; however, parents can also affect offspring fitness by indirect genetic and environmental routes. The life history strategy that an individual adopts will be influenced by both genes and environment; and this may have important consequences for offspring. Recent research has linked telomere dynamics (i.e., telomere length and loss) in early life to future viability and longevity. Moreover, a number of studies have reported a heritable component to telomere length across a range of vertebrates, although the effects of other parental contribution pathways have been far less studied. Using wild Atlantic salmon with different parental life histories in an experimental split‐brood in vitro fertilization mating design and rearing the resulting families under standardized conditions, we show that there can be significant links between parental life history and offspring telomere length (studied at the embryo and fry stage). Maternal life history traits, in particular egg size, were most strongly related to offspring telomere length at the embryonic stage, but then became weaker through development. In contrast, paternal life history traits, such as the father's growth rate in early life, had a greater association in the later stages of offspring development. However, offspring telomere length was not significantly related to either maternal or paternal age at reproduction, nor to paternal sperm telomere length. This study demonstrates both the complexity and the importance of parental factors that can influence telomere length in early life.     

Parental and genetic factors rather than nesting forest patch size affect physiological traits of offspring in an area‐sensitive passerine: an experimental study

Our understanding of the effects of habitat loss on individual performance is limited due to a lack of experimental studies that take the potential genetic and parental effects producing phenotypic variation into consideration. To assess the relative role of habitat loss on offspring phenotype while controlling for the confounding effects of genetic and parental variation we performed a partial cross‐fostering experiment using the Eurasian Treecreeper Certhia familiaris. The experiment was carried out by swapping half the nestlings in a brood between small and large nesting forest patches to determine the effect of nesting forest patch size on five nestling traits reflecting morphological size, body condition, physiological stress and inflammation status. There was no effect of nesting forest patch size on the offspring traits examined. Instead, we found evidence of genetic and early parental effects on all traits except inflammation status, as well as parental effects after cross‐fostering for all of the measured offspring traits. Our results suggest that genetic and parental effects should be taken into account when making inferences about species’ responses to habitat loss.     

Maternal and paternal contributions to egg size and egg number variation in the blackfin pearl killifish <Emphasis Type="Italic">Austrolebias nigripinnis</Emphasis>

Reproductive effort, egg number and egg size are traditionally considered to be ‘female’ life history traits. However, females often adjust the amount of resources allocated to reproduction depending on their mate, causing male environmental effects on life history traits. If females respond to male traits which are genetically variable, then male environmental effects contain indirect genetic effects. Estimates of how much of the total variation in life history traits originates from female effects versus male environmental effects, seems mostly lacking. We have investigated variation in rates of egg production and in egg size in the annual Argentinian blackfin pearl killifish Austrolebias nigripinnis, in a crossed design where males were exchanged repeatedly between females. Our analysis of phenotypic variance components of reproductive effort, egg size and egg number indicates that the amount of variation contributed by male environmental effects is equal (egg size, reproductive effort) or larger (egg number) than that between females. For egg size and number, we find that male environmental effects consist of a male random effect representing the average response of females to male phenotype, plus a female-male interaction term. This term can be understood as the deviation from the population mean of an individual female’s response. For reproductive effort, we find that the male environmental effect consists of an interaction term only. Random effects on egg size and number additionally vary in magnitude depending on the weekday where we collected eggs, probably due to cyclic variation in experimental conditions. Since we find that both male phenotype and environmental conditions affect egg size and number as determined by females, our results suggest that selection on these life history traits will be frequency-dependent.     

Males influence maternal effects that promote sexual selection: a quantitative genetic experiment with dung beetles Onthophagus taurus

Recently, doubt has been cast on studies supporting good genes sexual selection by the suggestion that observed genetic benefits for offspring may be confounded by differential maternal allocation. In traditional analyses, observed genetic sire effects on offspring phenotype may result from females allocating more resources to the offspring of attractive males. However, maternal effects such as differential allocation may represent a mechanism promoting genetic sire effects, rather than an alternative to them. Here we report results from an experiment on the horned dung beetle Onthophagus taurus, in which we directly compare genetic sire effects with maternal effects that are dependent on sire phenotype. We found strong evidence that mothers provide more resources to offspring when mated with large-horned males. There were significant heritabilities for both horn length and body size, but when differential maternal effects were controlled, the observed estimates of genetic variance were greatly reduced. Our experiment provides evidence that differential maternal effects may amplify genetic effects on offspring traits that are closely related to fitness. Thus, our results may partly explain the relatively high coefficients of additive genetic variation observed in fitness-related traits and provide empirical support for the theoretical argument that maternal effects can play an important role in evolution.     

Size‐induced phenotypic reaction norms in a parasitoid wasp: an examination of life‐history and behavioural traits

The amount of resources available during development often affects body size, causing phenotypic variation in life‐history traits and reproductive behaviours. However, past studies have seldom examined the reaction norms of both life‐history and behavioural traits versus body size. We measured the phenotypic plasticity of several life‐history (age‐specific egg load, egg size, longevity) and behavioural (oviposition rate, host marking rate, walking speed) traits of the egg parasitoid Telenomus podisi Ashmead (Hymenoptera: Scelionidae) in response to body size variation. We predicted that life‐history traits would show more evidence of size compensation than behavioural traits, resulting in fewer positively‐sloped size versus trait reaction norms among the former. As predicted by life‐history models, smaller wasps appear to shift resource allocation towards early‐life reproduction, having a similar egg load to large individuals 9 days after emergence. Surprisingly, longevity was unaffected by body size. However, egg size, the number of offspring produced during oviposition bouts, and the rate of subsequent egg synthesis were greater for larger individuals. In addition, as predicted, the reaction norms of behavioural traits versus body size were all positively sloped. Thus, despite possible adaptive compensatory plasticity of life‐history traits by small individuals, behavioural constraints directly related to body size would contribute to maintaining a positive size–fitness relationship.     

Dietary effects on life history traits in a terrestrial isopod: the importance of evaluating maternal effects and trade-offs

Studies of life history aim to explain patterns in the evolution of reproductive investment, growth, and survival. Trade-offs between traits are a fundamental component of life history theory. In herbivorous arthropods life history traits are often responsive to variation in numerous environmental factors, especially diet quality. Using three artificial diets under controlled laboratory conditions, we examined changes in life history traits (i.e. growth rate, offspring number, offspring size, incubation period), trade-offs between traits, and maternal effect on the growth rate of offspring, in the common woodlouse (terrestrial isopod), Porcellio laevis. The high protein diet had significant impacts on offspring production, triggering a smaller-sized offspring, and demonstrating a trade-off between these last two traits. The high carbohydrate diet seldom exerted a significant effect on incubation period. The quality of dietary items evidently has important consequences on the life history of the mother and, thus, on offspring growth; the directions of these effects, however, were opposite. Mothers fed diets with high protein concentrations presented significant maternal effects, measured as offspring growth rate during later ontogeny. Our results support the notion that protein, rather than carbohydrate, concentrations in the diet limit herbivorous arthropods, and have significant consequences on life history traits, as was seen for P. laevis. Clearly, the change in phenotypic correlations between incubation period and offspring number from negative to positive is an empirical demonstration of the context dependence of life history trait trade-offs.     

Genetic and Maternal Effects on Offspring Mortality in Mice

Trade-offs occur when two traits have opposing fitness effects such that positive selection on one trait is constrained by the negative fitness consequences of the other trait. To understand why trade-off may arise we need to study the genetic and non-genetic factors that influence associated traits because these may respond differently to selective pressure. Research into trade-offs has largely focused on the genetic basis of associated traits, yet both maternal effects and epigenetic effects have recently been shown to affect life history traits that play a role in trade-offs. In this study, we analyze genetic, epigenetic and life-history predictors of one of the most important trade-offs, that between offspring number and offspring mortality. Using a large-scale 3-generational intercross between two divergent mouse lines C57BL/6J and DBA/2J, we show that litter size differences between these lines, although significant, are surprisingly not the most important predictors of mortality. Offspring genotype, maternal effects and their interactions are the most influential factors determining mortality. We found significant paternal effects suggesting an important influence of paternal care or potentially the role of imprinted genes. Perhaps contrary to expectations our results further show that the trade-off between offspring number and mortality is not just a simple function of the two factors yielding, on average, an ‘optimal’ litter size at weaning. Indeed if one focused on litter size and mortality alone, the slope of relationship is the same for the two lines, yet they differ in the number of young at weaning. Our study reveals that a perceived trade-off between two traits is governed by a more complex set of interactions between genetic and non-genetic effects.     

Revisiting telegony: offspring inherit an acquired characteristic of their mother's previous mate

Newly discovered non‐genetic mechanisms break the link between genes and inheritance, thereby also raising the possibility that previous mating partners could influence traits in offspring sired by subsequent males that mate with the same female (‘telegony’). In the fly Telostylinus angusticollis, males transmit their environmentally acquired condition via paternal effects on offspring body size. We manipulated male condition, and mated females to two males in high or low condition in a fully crossed design. Although the second male sired a large majority of offspring, offspring body size was influenced by the condition of the first male. This effect was not observed when females were exposed to the first male without mating, implicating semen‐mediated effects rather than female differential allocation based on pre‐mating assessment of male quality. Our results reveal a novel type of transgenerational effect with potential implications for the evolution of reproductive strategies.     

A search for trade-offs among life history traits inDrosophila melanogaster

Summary Are there underlying developmental and physiological properties of organisms that can be used to build a general theory of life history evolution? Much of the theoretical work on the evolution of life histories is based on the premise of negative developmental and genetic correlations among life history traits. If negative correlations do not exist as a general rule then no general theory taking them into account is possible. Negative genetic correlations among life history traits can come about by antagonistic pleiotropy. One cause of antagonistic pleiotropy is cost allocation trade-offs. Since cost allocation trade-offs are due to underlying physiological constraints they are expected to be common to closely related groups. A second form of antagonistic pleiotropy is specialization of genotypes to different niches. This type of antagonistic pleiotropy is expected to be specific to each population. We looked for trade-offs in life history traits of longevity and fecundity inDrosophila melanogaster. We used a half-sib mating design and raised the offspring at two temperatures, 19°C and 25°C. Correlations between longevity and fecundity showed some evidence of antagonistic pleiotropy at high temperature with no evidence of any trade-offs at low temperature. Correlations of early and late fecundity traits did show evidence of cost allocation trade-offs at both temperatures. Antagonistic pleiotropy was also found for cross-environmental correlations of fecundity traits. We conclude that, although life history trade-offs can not be generally assumed, they are frequently found among functionally related traits. Thus, we provide guidelines for the development of general theories of life history evolution.     

Paternal body size affects reproductive success in laboratory-held zebrafish (<Emphasis Type="Italic">Danio rerio</Emphasis>)

Across many fish species, large females tend to exhibit higher individual reproductive success due to elevated fecundity and the provisioning of better conditioned eggs and offspring compared to small females. By contrast, effects of paternal body size on reproductive success are less well understood. We disentangled the maternal- and paternal-size dependent effects on reproductive output and early life history in zebrafish (Danio rerio). In the laboratory, females and males from four size categories (small, medium-sized, large and very large) were allowed to spawn freely in a full factorial design with 10 replicates per size combination. As expected, larger females produced more eggs and better conditioned offspring compared to smaller females. Male body size further contributed to zebrafish reproductive success: offspring sired by large males exhibited higher hatching probability and these offspring also hatched earlier and larger than offspring fertilized by small males. However, the largest males experienced lower mating success and received fewer eggs than males of the smaller size classes. While male body size substantially affected reproductive success in zebrafish, it remained unclear whether and to what degree direct paternal effects (e.g., related to sperm quality) or indirect paternal effects stemming from differential allocation patterns by females were the mechanism behind our findings. Answering this question constitutes an important future research topic.     

Parasites favour intermediate nestling mass and brood size in cliff swallows

A challenge of life‐history theory is to explain why animal body size does not continue to increase, given various advantages of larger size. In birds, body size of nestlings and the number of nestlings produced (brood size) have occasionally been shown to be constrained by higher predation on larger nestlings and those from larger broods. Parasites also are known to have strong effects on life‐history traits in birds, but whether parasitism can be a driver for stabilizing selection on nestling body size or brood size is unknown. We studied patterns of first‐year survival in cliff swallows (Petrochelidon pyrrhonota) in western Nebraska in relation to brood size and nestling body mass in nests under natural conditions and in those in which hematophagous ectoparasites had been removed by fumigation. Birds from parasitized nests showed highest first‐year survival at the most common, intermediate brood‐size and nestling‐mass categories, but cliff swallows from nonparasitized nests had highest survival at the heaviest nestling masses and no relationship with brood size. A survival analysis suggested stabilizing selection on brood size and nestling mass in the presence (but not in the absence) of parasites. Parasites apparently favour intermediate offspring size and number in cliff swallows and produce the observed distributions of these traits, although the mechanisms are unclear. Our results emphasize the importance of parasites in life‐history evolution.     

Female freshwater crayfish adjust egg and clutch size in relation to multiple male traits

Females may invest more in reproduction if they acquire mates of high phenotypic quality, because offspring sired by preferred partners may be fitter than offspring sired by non-preferred ones. In this study, we tested the differential maternal allocation hypothesis in the freshwater crayfish, Austropotamobius italicus, by means of a pairing experiment aimed at evaluating the effects of specific male traits (body size, chelae size and chelae asymmetry) on female primary reproductive effort. Our results showed that females laid larger but fewer eggs for relatively small-sized, large-clawed males, and smaller but more numerous eggs for relatively large-sized, small-clawed males. Chelae asymmetry had no effects on female reproductive investment. While the ultimate consequences of this pattern of female allocation remain unclear, females were nevertheless able to adjust their primary reproductive effort in relation to mate characteristics in a species where inter-male competition and sexual coercion may mask or obscure their sexual preferences. In addition, our results suggest that female allocation may differentially affect male characters, thus promoting a trade-off between the expression of different male traits.     

The combined effect of host and food availability on optimized parasitoid life‐history traits based on a three‐dimensional trade‐off surface

The reproductive success of many insects is considered to be limited by two main factors: the availability of mature eggs to lay (termed egg limitation) and the time to locate suitable hosts (termed time limitation). High host density in the environment is likely to enhance oviposition opportunities, thereby selecting for higher investment in egg supply. In contrast, a shortage of food (e.g. sugar sources) is likely to increase the risk of time limitation, thereby selecting for higher allocation to initial energy reserves. To our knowledge, the combined effect of host and food availability on these optimal life‐history allocations has never been investigated. We thus modelled their simultaneous effects on a three‐dimensional trade‐off between initial investment in energy reserves, egg number and egg size, while focusing on insect parasitoids. The model was based on Monte Carlo simulations coupled with genetic algorithms, in order to identify the optimal life‐history traits of a single simulated parasitoid female in an environment in which both hosts and food are present in varying densities. Our results reproduced the simple predictions described above. However, some novel predictions were also obtained, especially when specific interactions between the different factors were examined and their effects on the three‐dimensional life‐history surface were considered. The work sheds light on long‐lasting debates regarding the relative importance of time versus egg limitation in determining insect life‐history traits and highlights the complexity of life‐history evolution, where several environmental factors act simultaneously on multiple traits.     

Consequences of hierarchical allocation for the evolution of life-history traits

Resource allocation within individuals may often be hierarchical, and this may have important effects on genetic correlations and on trait evolution. For example, organisms may divide energy between reproduction and somatic growth and then subdivide reproductive resources. Genetic variation in allocation to pathways early in such hierarchies (e.g., reproduction) can cause positive genetic correlations between traits that trade off (e.g., offspring size and number) because some individuals invest more resources in reproduction than others. We used quantitative-genetic models to explore the evolutionary implications of allocation hierarchies. Our results showed that when variation in allocation early in the hierarchy exceeds subsequent variation in allocation, genetic covariances and initial responses to selection do not reflect trade-offs occurring at later levels in the hierarchy. This general pattern was evident for many starting allocations and optima and for whether traits contributed multiplicatively or additively to fitness. Finally, artificial selection on a single trait revealed masked trade-offs when variation in early allocation was comparable to subsequent variation in allocation. This result confirms artificial selection as a powerful, but not foolproof, method of detecting trade-offs. Thus, allocation hierarchies can profoundly affect life-history evolution by causing traits to evolve in the opposite direction to that predicted by trade-offs.     

Viability selection on early body mass and the effect of female body size on fecundity: a study on the leaf-eared mouse <Emphasis Type="Italic">Phyllotis darwini</Emphasis>

Viability selection and fecundity of size-related traits has been demonstrated to be strong in vertebrates. In small mammals, both offspring and adult size are important for viability and fecundity, respectively. We studied the role of early phenotypic selection on size attributes and female fecundity in the leaf-eared mouse (Phyllotis darwini). Our results support that larger females produce more offspring, and since the likelihood of attaining adulthood is similar for different sizes of the females, those larger females also produce more offspring that attain sexual maturity. From the offspring perspective, larger pups at birth have significantly more probability of attaining sexual maturity. However, weaning mass and growth rate did not show any differential survival. Our study suggests that early selection could be important and could prevent further episodes of selection by early culling of the distribution of sizes, and that “effective” fecundity is strongly dependent on the size of the female.     

What happens to offspring when parents are inbred,old or had a poor start in life? Evidence for sex‐specific parental effects

Parental effects on offspring performance have been attributed to many factors such as parental age, size and condition. However, we know little about how these different parental characteristics interact to determine parental effects, or the extent to which their effect on offspring depends on either the sex of the parent or that of the offspring. Here we experimentally tested for effects of variation in parents’ early diet and inbreeding levels, as well as effects of parental age, and for potential interactive effects of these three factors on key aspects of offspring development in the mosquitofish (Gambusia holbrooki). Older mothers produced offspring that were significantly smaller at birth. This negative effect of maternal age on offspring size was still evident at maturation as older mothers had smaller daughters, but not smaller sons. The daughters of older mothers did, however, reach maturity sooner. Paternal age did not affect offspring body size, but it had a complex effect on their sons’ relative genital size. When initially raised on a food‐restricted diet, older fathers sired sons with relatively smaller genitalia, but when fathers were initially raised on a control diet their sons had relatively larger genitalia. The inbreeding status of mothers and fathers had no significant effects on any of the measured offspring traits. Our results indicate that the manifestation of parental effects can be complex. It can vary with both parent and offspring sex; can change over an offspring's life; and is sometimes evident as an interaction between different parental traits. Understanding this complexity will be important to predict the role of parental effects in adaptation.     

Decreased sexual signalling reveals reduced viability in small populations of the drumming wolf spider Hygrolycosa rubrofasciata

One of the important goals in conservation biology is to determine reliable indicators of population viability. Sexual traits have been suggested to indicate population extinction risk, because they may be related to viability through condition dependence. Moreover, condition-dependent sexual traits may be more sensitive indicators of population viability than early life-history traits, because deleterious fitness effects of inbreeding tend to be expressed mainly at the end of the species' life history. However, empirical evidence of the significance of sexual behaviour for population viability is missing. In this study, we examined two male sexual traits and survival in 39 different-sized and isolated natural populations of the wolf spider, Hygrolycosa rubrofasciata. We also used several traits to estimate female reproductive success in 25 populations of H. rubrofasciata. According to previous studies, H. rubrofasciata males have a costly and condition-dependent acoustic signal, courtship drumming, which is the target of female choice. Males with a high drumming rate have considerably higher viability than males with a low drumming rate, and females that mate with the more actively drumming males gain genetic benefits in terms of increased offspring viability. Our results show that males in small populations had both lower survival and lower drumming rate than males in larger populations. However, we did not find any evidence for a decline in important early life-history traits (offspring number, hatching success or offspring body mass) or female body mass in small populations. Our results have two important messages for conservation biology. First, they show that sexual traits can be used as sensitive indicators of population viability. Second, the indirect benefits of female choice in terms of good genes might partially compensate for the reduction of viability in declining populations. Also, our results support the view that deleterious effects of small population size are expressed at the end of the species' life history.