Differential effects of offspring and maternal inbreeding on egg laying and offspring performance in the burying beetle Nicrophorus vespilloides

We investigate the effect of offspring and maternal inbreeding on maternal and offspring traits associated with early offspring fitness in the burying beetle Nicrophorus vespilloides. We conducted two experiments. In the first experiment, we manipulated maternal inbreeding only (keeping offspring outbred) by generating mothers that were outbred, moderately inbred or highly inbred. Meanwhile, in the second experiment, we manipulated offspring inbreeding only (keeping females outbred) by generating offspring that were outbred, moderately inbred or highly inbred. In both experiments, we monitored subsequent effects on breeding success (number of larvae), maternal traits (clutch size, delay until laying, laying skew, laying spread and egg size) and offspring traits (hatching success, larval survival, duration of larval development and average larval mass). Maternal inbreeding reduced breeding success, and this effect was mediated through lower hatching success and greater larval mortality. Furthermore, inbred mothers produced clutches where egg laying was less skewed towards the early part of laying than outbred females. This reduction in the skew in egg laying is beneficial for larval survival, suggesting that inbred females adjusted their laying patterns facultatively, thereby partially compensating for the detrimental effects of maternal inbreeding on offspring. Finally, we found evidence of a nonlinear effect of offspring inbreeding coefficient on number of larvae dispersing. Offspring inbreeding affected larval survival and larval development time but also unexpectedly affected maternal traits (clutch size and delay until laying), suggesting that females adjust clutch size and the delay until laying in response to being related to their mate.     

The inbreeding depression cost of selfing: Importance of flower size and population size in Collinsia parviflora (Veronicaceae)

Inbreeding depression should evolve with selfing rate when frequent inbreeding results in exposure of and selection against deleterious alleles. The selfing rate may be modified by plant traits such as flower size, or by population characteristics such as census size that can affect the probability of biparental inbreeding. Here we quantify inbreeding depression (δ) among different population sizes of Collinsia parviflora, a wildflower with interpopulation variation in flower size, by comparing fitness components and multiplicative fitness of experimentally produced selfed and outcrossed offspring. Selfed offspring had reduced multiplicative fitness compared to outcrossed offspring, but inbreeding depression was low in all combinations of population size and flower size (δ ≤ 0.05) except in large populations of large-flowered plants (δ = 0.45). The decrement to multiplicative fitness with inbreeding was not affected by population size nested within flower size, but differed between small- and large-flowered plants: small-flowered populations had lower overall inbreeding depression (δ = 0.04) compared to large-flowered populations (δ = 0.25). The difference in load with flower size suggests that either selection has removed deleterious recessive alleles or these alleles have become fixed in small-flowered, potentially more selfing populations, but that purging has not occurred to the same extent in presumably outcrossing large-flowered populations.     

CORRELATED EVOLUTION OF MATING STRATEGY AND INBREEDING DEPRESSION WITHIN AND AMONG POPULATIONS OF THE HERMAPHRODITIC SNAIL PHYSA ACUTA

Inbreeding depression is one of the main forces opposing the evolution of self-fertilization. Of central importance is the hypothesis that inbreeding depression and selfing coevolve antagonistically, generating either low selfing rate and high inbreeding depression or vice versa. However, there is limited evidence for this coevolution within species. We investigated this topic in the hermaphroditic snail Physa acuta . In this species, isolated individuals delay the onset of egg laying compared to individuals having access to mates. Longer delays ("waiting times") indicate more intense selfing avoidance. We measured inbreeding depression and waiting time in a large quantitative-genetic experiment (281 outbred families derived from 26 natural populations). We observed large genetic variance for both traits and a strong positive genetic covariance between them, most of which resided within rather than among populations. It means that, within populations, individuals with higher mutation load avoided selfing more strongly on average. This genetic covariance may result from pleiotropy and/or linkage disequilibrium. Whatever its genetic architecture, the fact it emerges specifically when individuals are deprived of mates suggests it is not fortuitous and rather reflects the action of natural selection. We conclude that a diversity of mating strategies can arise within populations subjected to variation in inbreeding depression.     

Comparative effects of inbreeding and outbreeding on the ontogeny of Heliconius erato phyllis (Lepidoptera: Nymphalidae)

Inbreeding depression has been reported in various groups of organisms, including insects. Estimates of inbreeding consequences were obtained by comparing 12 life‐history and morphological traits among nine inbred families (F = 0.25) and 16 outbred families (F = 0) of the Neotropical butterfly Heliconius erato phyllis. A Student's t‐test showed statistically significant differences for pupal weight and right forewing area, both in males and in females, between inbred and outbred families. Survival during development, from egg hatching to adulthood, also differed significantly between inbred and outbred families. The average number of haploid lethal equivalents was 0.17 for pupal weight, 0.15 for forewing area and 0.71 for survival from hatching to adulthood. The results of this study confirm that the consequences of inbreeding are more deleterious to life history traits than to morphological ones.     

The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster

We performed a large-scale experiment on the effects of inbreeding and population bottlenecks on the additive genetic and environmental variance for morphological traits in Drosophila melanogaster. Fifty-two inbred lines were created from the progeny of single pairs, and 90 parent-offspring families on average were measured in each of these lines for six wing size and shape traits, as well as 1945 families from the outbred population from which the lines were derived. The amount of additive genetic variance has been observed to increase after such population bottlenecks in other studies; in contrast here the mean change in additive genetic variance was in very good agreement with classical additive theory, decreasing proportionally to the inbreeding coefficient of the lines. The residual, probably environmental, variance increased on average after inbreeding. Both components of variance were highly variable among inbred lines, with increases and decreases recorded for both. The variance among lines in the residual variance provides some evidence for a genetic basis of developmental stability. Changes in the phenotypic variance of these traits are largely due to changes in the genetic variance.     

Genetic and environmental sources of egg size, fecundity and body size in the migrant skipper, Parnara guttata guttata (Lepidoptera: Hesperiidae)

Genetic and environmental sources of egg size, fecundity and body size (forewing length) were examined in the butterfly, Parnara guttata guttata. Phenotypic and genetic correlation and heritability were estimated for these traits under different day-length and temperature conditions. Egg size and fecundity had relatively high heritabilities, and body sizes in males and females had moderate and high heritability, respectively. Negative phenotypic and genetic correlations between egg size and fecundity were estimated in treatments corresponding to the natural conditions during larval development of the first and second generations. Phenotypic and genetic correlations between body size and egg size differed considerably between insects reared under long and short day-lengths. Next, genotype–environment interactions were estimated by comparing reaction norms to day-length or temperature of these traits among families. ANOVA analysis revealed significant genotype–environment interactions in egg size and forewing length in both sexes for day-length and temperature. These results suggested that a large additive genetic variance for egg size might have been maintained by a genetic trade-off and/or by genotype–environment interactions in P. g. guttata.     

Inbreeding and adaptive plasticity: an experimental analysis on predator‐induced responses in the water flea Daphnia

Several studies have emphasized that inbreeding depression (ID) is enhanced under stressful conditions. Additionally, one might imagine a loss of adaptively plastic responses which may further contribute to a reduction in fitness under environmental stress. Here, we quantified ID in inbred families of the cyclical parthenogen Daphnia magna in the absence and presence of fish predation risk. We test whether predator stress affects the degree of ID and if inbred families have a reduced capacity to respond to predator stress by adaptive phenotypic plasticity. We obtained two inbred families through clonal selfing within clones isolated from a fish pond. After mild purging under standardized conditions, we compared life history traits and adaptive plasticity between inbred and outbred lineages (directly hatched from the natural dormant egg bank of the same pond). Initial purging of lineages under standardized conditions differed among inbred families and exceeded that in outbreds. The least purged inbred family exhibited strong ID for most life history traits. Predator‐induced stress hardly affected the severity of ID, but the degree to which the capacity for adaptive phenotypic plasticity was retained varied strongly among the inbred families. The least purged family overall lacked the capacity for adaptive phenotypic plasticity, whereas the family that suffered only mild purging exhibited a potential for adaptive plasticity that was comparable to the outbred population. We thus found that inbred offspring may retain the capacity to respond to the presence of fish by adaptive phenotypic plasticity, but this strongly depends on the parental clone engaging in selfing.     

High variability in egg size and energetic content among intertidal mussels

Maternal investment is a fundamentally important parameter in life-history theory and models, yet the scales at which it varies (among individuals vs. among populations) is rarely reported. In this study, variability in attributes of eggs and early larvae of Mytilus californianus was examined from four sites spanning Point Conception, California, in June and September 2001. The effects of female, site, and month were examined for the following variables: egg volume (microl), egg energy content (microg carbon per egg), and initial larval size (microm). The only significant effect on both egg traits was that of female. Females differed by up to 57% in mean egg volume and 116% in mean egg energetic content. Although there were significant effects of rearing environment, female, site, and month on initial larval size, variability in larval length was small compared to the egg traits. Mean larval length was maximally 11% different among females. Neither female body weight nor length was correlated to mean offspring traits, and there were also no significant relationships between egg traits and initial larval size. The primary source of variation in maternal investment in this system appears to be among individual females rather than over space or time.     

SEXUAL TRAITS ARE SENSITIVE TO GENETIC STRESS AND PREDICT EXTINCTION RISK IN THE STALK‐EYED FLY,DIASEMOPSIS MEIGENII

The handicap principle predicts that sexual traits are more susceptible to inbreeding depression than nonsexual traits. However, this hypothesis has received little testing and results are inconsistent. We used 11 generations of full‐sibling mating to test the effect of inbreeding on sexual and nonsexual traits in the stalk‐eyed fly Diasemopsis meigenii. Consistent with the theoretical predictions, the male sexual trait (eyespan) decreased more than nonsexual traits (female eyespan and male wing length), even after controlling for body size variation. In addition, male eyespan was a reliable predictor of line extinction, unlike other nonsexual traits. After 11 generations, inbred lines were crossed to generate inbred and outbred families. All morphological traits were larger in outbred individuals than inbred individuals. This heterosis was greater in male eyespan than in male wing length, but not female eyespan. The elevated response in male eyespan to genetic stress mirrored the result found using environmental stress during larval development and suggests that common mechanisms underlie the patterns observed. Overall, these results support the hypothesis that male sexual traits suffer more from inbreeding depression than nonsexual traits and are in line with predictions based on the handicap principle.     

Juvenile hormone mediates a trade-off between primary and secondary sexual traits in stalk-eyed flies

Trade-offs between developing body parts may contribute to variation in allometric scaling relationships in a variety of taxa. Experimental evidence indicates that both circulating levels of juvenile hormone (JH) and sensitivities of developing body parts to JH can influence morphology in polyphenic insects. However, the extent to which JH may regulate both the development of traits that scale continuously with body size and trade-offs between these traits is largely unknown. Here, I present evidence that the JH analog methoprene applied to final instar larvae of a stalk-eyed fly (Cyrtodiopsis dalmanni) can induce males to produce larger eye-stalks relative to their body size. Examination of testis growth, sperm transfer, and egg maturation indicates that JH induces a trade-off between eye-span and gonad development in adult males, but not females. Age at sexual maturity was unaffected by larval JH applications to either sex. Collectively, these results are consistent with JH-mediated allocation of resources to eye-span at the expense of testes, and indicate potential costs for the production of an exaggerated trait.     

INBREEDING DEPRESSION IN HYDROPHYLLUM APPENDICULATUM: ROLE OF MATERNAL EFFECTS,CROWDING, AND PARENTAL MATING HISTORY

This paper examines several aspects of the expression of inbreeding depression in an outcrossing, obligately biennial plant, Hydrophyllum appendiculatum (Hydrophyllaceae). The amount of inbreeding depression detected was small during the first year of life but increased with age and had significant effects on adult size and reproductive traits. The lack of significant inbreeding depression during early growth is likely due to the overriding influence of maternal environmental effects on seed size and seedling growth. However, as maternal effects decreased with age, the seedling's own genotype became a more important determinant of its fate. To examine whether the expression of inbreeding depression was sensitive to ecological conditions, selfed and outcrossed seedlings were grown alone or with other H. appendiculatum seedlings. No inbreeding depression was detected in the plants grown alone. In contrast, under competitive conditions, outcrossed seedlings were significantly larger than selfed seedlings by the end of the first growing season. To address whether parental mating history influences the amount of inbreeding depression expressed, I examined the consequences of two successive generations of selfing on seed set and seed weight. The amount of inbreeding depression increased following the second generation of selfing. In the first generation, seed set and seed weight differed by less than 5% between selfed and outcrossed progeny. However, both traits were 15% greater for outcrossed plants after two generations. These results indicate that the alleles responsible for the reductions in these traits were not purged and suggest the action of multiple loci with deleterious effects.     

Joint evolution of differential seed dispersal and self‐fertilization

Differential seed dispersal, in which selfed and outcrossed seeds possess different dispersal propensities, represents a potentially important individual‐level association. A variety of traits can mediate differential seed dispersal, including inflorescence and seed size variation. However, how natural selection shapes such associations is poorly known. Here, we developed theoretical models for the evolution of mating system and differential seed dispersal in metapopulations, incorporating heterogeneous pollination, dispersal cost, cost of outcrossing and environment‐dependent inbreeding depression. We considered three models. In the ‘fixed dispersal model’, only selfing rate is allowed to evolve. In the ‘fixed selfing model’, in which selfing is fixed but differential seed dispersal can evolve, we showed that natural selection favours a higher, equal or lower dispersal rate for selfed seeds to that for outcrossed seeds. However, in the ‘joint evolution model’, in which selfing and dispersal can evolve together, evolution necessarily leads to higher or equal dispersal rate for selfed seeds compared to that for outcrossed. Further comparison revealed that outcrossed seed dispersal is selected against by the evolution of mixed mating or selfing, whereas the evolution of selfed seed dispersal undergoes independent processes. We discuss the adaptive significance and constraints for mating system/dispersal association.     

LIFETIME INBREEDING DEPRESSION,PURGING, AND MATING SYSTEM EVOLUTION IN A SIMULTANEOUS HERMAPHRODITE TAPEWORM

Classical theory on mating system evolution suggests that simultaneous hermaphrodites should either outcross if they have high inbreeding depression (ID) or self‐fertilize if they have low ID. However, a mixture of selfing and outcrossing persists in many species. Previous studies with the tapeworm Schistocephalus solidus have found worms to self‐fertilize some of their eggs despite ID. The probability for selfing to spread depends on the relative fitness of selfers, as well as the genetic basis for ID and whether it can be effectively purged. We bred S. solidus through two consecutive generations of selfing and recorded several fitness correlates over the whole life cycle. After one round of selfing, ID was pronounced, particularly in early‐life traits, and the conservatively estimated lifetime fitness of selfed progeny was only 9% that of the outcrossed controls. After a second generation of selfing, ID remained high but was significantly reduced in several traits, which is consistent with the purging of deleterious recessive alleles (the estimated load of lethal equivalents dropped by 48%). Severe ID, even if it can be rapidly purged, likely prevents transitions toward pure selfing in this parasite, although we also cannot exclude the possibility that low‐level selfing has undetected benefits.     

Effects of inbreeding on male function and self-fertility in the partially self-incompatible herb Campanula rapunculoides (Campanulaceae)

We examined the effect of inbreeding on fitness (through both male and female functions) and changes in self-fertility in the partially self-incompatible species Campanula rapunculoides. Individuals in natural populations of C. rapunculoides varied extensively in their strength of self-incompatibility (SI). We crossed 11 individuals that differed in their strength of SI to generate families with four levels of inbreeding (f = 0.0, 0.25, 0.5, and 0.75). Progeny were scored for three traits related to male fitness and for outcrossed and selfed seed production. Analyses of variance revealed significant inbreeding depression for the three male traits and seed set. Families with strong or weak SI differed in their response to inbreeding. Families with weak SI had lower levels of inbreeding depression for most traits than families with strong SI, but strong SI families had a greater increase in selfed seed set, but not self-fertility, with inbreeding. Finally, we found evidence of a significant linear response to inbreeding for all three male reproductive traits and outcrossed seed, indicating that inbreeding depression was primarily caused by partially or fully recessive deleterious alleles. Variation in genetic load was associated with variation in self-fertility, a finding that suggests an evolutionary role for partial self-fertility in natural populations of C. rapunculoides.     

Parental effects on embryonic viability and growth in Arctic charr Salvelinus alpinus at two incubation temperatures

The parental influences on three progeny traits (survival to eyed‐embryo stage, post‐hatching body length and yolk‐sac volume) of Arctic charr Salvelinus alpinus were studied under two thermal conditions (2 and 7° C) using a factorial mating design. The higher temperature resulted in elevated mortality rates and less advanced development at hatching. Survival was mostly attributable to maternal effects at both temperatures, but the variation among families was dependent on egg size only at the low temperature. No additive genetic variation (or pure sire effect) could be observed, whereas the non‐additive genetic effects (parental combination) contributed to offspring viability at 2° C. In contrast, any observable genetic variance in survival was lost at 7° C, most likely due to the increased environmental variance. Irrespective of temperature, dam and sire–dam interaction contributed significantly to the phenotypic variation in both larval length and yolk size. A significant proportion of the variation in larval length was also due to the sire effect at 2° C. Maternal effects were mediated partly through egg size, but as a whole, they decreased in importance at the high temperature, enabling a concomitant increase in non‐additive genetic effects. For larval length, however, the additive component, like maternal effects, decreased at 7° C. The present results suggest that an exposure to thermal stress during incubation can modify the genetic architecture of early developmental traits in S. alpinus and presumably constrain their short‐term adaptive potential and evolvability by increasing the amount of environmentally induced variation.     

Influence of selfing and maternal effects on life-cycle traits and dispersal ability in the herb Hypochaeris radicata (Asteraceae)

The ecological and evolutionary implications of dispersal are many. Pollination type and maternal effects may affect plant fitness traits, including life-cycle traits as well as dispersal ability. This study investigated the joint influence of pollination type and maternal effects on both life-cycle traits and dispersal ability in the herb Hypochaeris radicata . We conducted experimental crosses to obtain selfed and outcrossed progeny. Individual seeds and their pappuses were measured to determine seed terminal velocity. Seed size was also used to assess maternal effects. Selfing dramatically decreased seed set, indicating that H. radicata is self-incompatible. However, the few selfed seeds produced outperformed outcrossed seeds in seed size and flowering probability, surely as a result of an effective reallocation of resources among selfed seeds. None of the life-cycle traits was affected by seed size, the estimate of maternal effects. Selfed seeds were larger and bore a smaller pappus than outcrossed seeds. As a result, dispersal ability was lower for selfed than outcrossed seeds. Several factors, such as the low proportion of plants that produced selfed seeds, the low number of selfed seeds produced per plant, and the lack of self-fertility mechanisms might act in concert to prevent the evolution of selfing in H. radicata .  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 146 , 163–170.     

Control and Consequences of Alternative Developmental Modes in a Poecilogonous Polychaete

SYNOPSIS. The poecilogonous polychaete Streblospio benedicti(Webster) exhibits both planktotrophic and lecithotrophic modesof larval development. The alternative trophic modes are associatedwith differences in age and size at maturation, offspring number,size and energetic investment, larval planktonic period, morphologyand survivorship. This paper reviews a decade of research intothe control and consequences of the traits associated with planktotrophyand lecithotrophy in S. benedicti. The dominant control on reproductiveand developmental characters is genetic. Significant additivegenetic variance has been detected for egg diameter, fecundity,larval planktonic period and aspects of larval morphology. However,environmental factors such as temperature, food quality andphotoperiod, and intrinsic factors such as maternal age, exertconsiderable influence on non-trophic developmental traits (e.g.,offspring number, size and energy content). Demographic consequencesof development mode are reviewed for field and laboratory demesof S. benedicti dominated by individuals exhibiting either planktotrophyor lecithotrophy. Similar population size structure, fluctuationsin abundance, P: B ratios, and estimated population growth ratesare achieved through trade-offs between survivorship and fecundity. Development mode may best be viewed as a complex set of traitsthat are intimately linked developmentally and evolutionarilyto other aspects of an organism's life history. Greater insightinto the control and consequences of development mode shouldresult from further investigation of these linkages     

Inbreeding,inbreeding depression and extinction

Inbreeding is unavoidable in small, isolated populations and can cause substantial fitness reductions compared to outbred populations. This loss of fitness has been predicted to elevate extinction risk giving it substantial conservation significance. Inbreeding may result in reduced fitness for two reasons: an increased expression of deleterious recessive alleles (partial dominance hypothesis) or the loss of favourable heterozygote combinations (overdominance hypothesis). Because both these sources of inbreeding depression are dependent upon dominance variance, inbreeding depression is predicted to be greater in life history traits than in morphological traits. In this study we used replicate inbred and control lines of Drosophila simulans to address three questions:1) is inbreeding depression greater in life history than morphological traits? 2) which of the two hypotheses is the major underlying cause of inbreeding depression? 3) does inbreeding elevate population extinction risk? We found that inbreeding depression was significantly greater in life history traits compared to morphological traits, but were unable to find unequivocal support for either the overdominance or partial dominance hypotheses as the genetic basis of inbreeding depression. As predicted, inbred lines had a significantly greater extinction risk.     

Two classes of deleterious recessive alleles in a natural population of zebrafish, Danio rerio

Natural populations carry deleterious recessive alleles which cause inbreeding depression. We compared mortality and growth of inbred and outbred zebrafish, Danio rerio, between 6 and 48 days of age. Grandparents of the studied fish were caught in the wild. Inbred fish were generated by brother-sister mating. Mortality was 9% in outbred fish, and 42% in inbred fish, which implies at least 3.6 lethal equivalents of deleterious recessive alleles per zygote. There was no significant inbreeding depression in the growth, perhaps because the surviving inbred fish lived under less crowded conditions. In contrast to alleles that cause embryonic and early larval mortality in the same population, alleles responsible for late larval and early juvenile mortality did not result in any gross morphological abnormalities. Thus, deleterious recessive alleles that segregate in a wild zebrafish population belong to two sharply distinct classes: early-acting, morphologically overt, unconditional lethals; and later-acting, morphologically cryptic, and presumably milder alleles.