Polyandry, life-history trade-offs and the evolution of imprinting at Mendelian loci

Genomic imprinting causes parental origin-dependent differential expression of a small number of genes in mammalian and angiosperm plant embryos, resulting in non-Mendelian inheritance of phenotypic traits. The "conflict" theory of the evolution of imprinting proposes that reduced genetic relatedness of paternally, relative to maternally, derived alleles in offspring of polygamous females supports parental sex-specific selection at gene loci that influence maternal investment. While the theory's physiological predictions are well supported by observation, the requirement of polyandry in the evolution of imprinting from an ancestral Mendelian state has not been comprehensively analyzed. Here, we use diallelic models to examine the influence of various degrees of polyandry on the evolution of both Mendelian and imprinted autosomal gene loci that influence trade-offs between maternal fecundity and offspring viability. We show that, given a plausible assumption on the physiological relationship between maternal fecundity and offspring viability, low levels of polyandry are sufficient to reinforce exclusively the fixation of "greedy" paternally imprinted alleles that increase offspring viability at the expense of maternal fecundity and "thrifty" maternally imprinted alleles of opposite effect. We also show that, for all levels of polyandry, Mendelian alleles at genetic loci that influence the trade-off between maternal fecundity and offspring viability reach an evolutionary stable state, whereas pairs of reciprocally imprinted alleles do not.     

DO EMBRYOS INFLUENCE MATERNAL INVESTMENT? EVALUATING MATERNAL‐FETAL COADAPTATION AND THE POTENTIAL FOR PARENT‐OFFSPRING CONFLICT IN A PLACENTAL FISH

The evolution of matrotrophy introduces the potential for genomic conflicts between mothers and embryos. These conflicts are hypothesized to accelerate the evolution of reproductive isolation and to influence the evolution of life-history traits, reproductive structures, and genomic imprinting. These hypotheses assume offspring can influence the amount of maternal investment they receive and that there is a trade-off between maternal investment into individual offspring and maternal survival or fecundity. We used field data and laboratory crosses to test whether these assumptions are met in the matrotrophic poeciliid fish Heterandria formosa . Comparisons of life histories between two natural populations demonstrated a trade-off between the level of maternal investment into individual embryos and maternal fecundity. Laboratory crosses between individuals from these populations revealed that offspring genotype exerts an influence on the level of maternal investment and affects maternal fecundity through higher rates of embryo abortion and lower numbers of full-term offspring. Our results show that the prerequisites for parent–offspring conflict to be a potent evolutionary force in poeciliid fish are present in H. formosa. However, determining whether this conflict has shaped maternal investment in nature will require disentangling any effects of conflict from those of several ecological factors that are themselves correlated with the expected intensity of conflict.     

The effect of genetic conflict on genomic imprinting and modification of expression at a sex-linked locus

We examine how genomic imprinting may have evolved at an X-linked locus, using six diallelic models of selection in which one allele is imprintable and the other is not. Selection pressures are generated by genetic conflict between mothers and their offspring. The various models describe cases of maternal and paternal inactivation, in which females may be monogamous or bigamous. When inactivation is maternal, we examine the situations in which only female offspring exhibit imprinting as well as when both sexes do. We compare our results to those previously obtained for an autosomal locus and to four models in which a dominant modifier of biallelic expression is subjected to the same selection pressures. We find that, in accord with verbal predictions, maternal inactivation of growth enhancers and paternal inactivation of growth inhibitors are more likely than imprinting in the respective opposite directions, although these latter outcomes are possible for certain parameter combinations. The expected outcomes are easier to evolve than the same outcomes for autosomal loci, contradicting the available evidence concerning the direction of imprinting on mammalian sex chromosomes. In most of our models stable polymorphism of imprinting status is possible, a behavior not predicted by verbal accounts.     

How effective are maternal effects at having effects?

The well studied trade-off between offspring size and offspring number assumes that offspring fitness increases with increasing per-offspring investment. Where mothers differ genetically or exhibit plastic variation in reproductive effort, there can be variation in per capita investment in offspring, and via this trade-off, variation in fecundity. Variation in per capita investment will affect juvenile performance directly--a classical maternal effect--while variation in fecundity will also affect offspring performance by altering the offsprings' competitive environment. The importance of this trade-off, while a focus of evolutionary research, is not often considered in discussions about population dynamics. Here, we use a factorial experiment to determine what proportion of variation in offspring performance can be ascribed to maternal effects and what proportion to the competitive environment linked to the size-number trade-off. Our results suggest that classical maternal effects are significant, but that in our system, the competitive environment, which is linked to maternal environments by fecundity, can be a far more substantial influence.     

Testing the imprinted brain: parent-of-origin effects on empathy and systemizing

Genomic imprinting is a violation of Mendel's laws that enables selection to act on genes, depending on parent of origin, but, even more controversially, on the sex of the offspring. This study tested whether there are parent-of-origin effects on the heritability of empathy and systemizing in the general population as part of a larger question concerning the role of imprinted genes in the evolution of human cognition and behaviour. The measures tested were the Empathy and Systemizing Quotients as proxies for the related terms mentalistic and mechanistic cognition in the imprinted brain theory.To test genomic imprinting hypotheses, correlations in behavioural scores between pairs of full, maternal and paternal siblings were compared. Where scores are influenced by imprinted genes, the actual correlations between pairs of siblings will differ from those expected following classical Mendelian inheritance in a predictable way depending on what kind of imprinting is influencing the trait. These theoretical predictions were used to test the fit of the data against Mendelian and imprinting models using structural equation modeling. The imprinted brain theory proposes a trade-off between maternally influenced mentalistic cognition and paternally influenced mechanistic cognition. However, the results of this study support a model of contrasting maternal and paternal influences on strong and weak empathizing and a maternal influence on systemizing. Although the sample size was insufficient to comprehensively analyse sex-limitation models, there is some evidence that heritability of systemizing is stronger in females than in males.     

A maternal-offspring coadaptation theory for the evolution of genomic imprinting

Imprinted genes are expressed either from the maternally or paternally inherited copy only, and they play a key role in regulating complex biological processes, including offspring development and mother–offspring interactions. There are several competing theories attempting to explain the evolutionary origin of this monoallelic pattern of gene expression, but a prevailing view has emerged that holds that genomic imprinting is a consequence of conflict between maternal and paternal gene copies over maternal investment. However, many imprinting patterns and the apparent overabundance of maternally expressed genes remain unexplained and may be incompatible with current theory. Here we demonstrate that sole expression of maternal gene copies is favored by natural selection because it increases the adaptive integration of offspring and maternal genomes, leading to higher offspring fitness. This novel coadaptation theory for the evolution of genomic imprinting is consistent with results of recent studies on epigenetic effects, and it provides a testable hypothesis for the origin of previously unexplained major imprinting patterns across different taxa. In conjunction with existing hypotheses, our results suggest that imprinting may have evolved due to different selective pressures at different loci.     

A Maternal–Offspring Coadaptation Theory for the Evolution of Genomic Imprinting

Imprinted genes are expressed either from the maternally or paternally inherited copy only, and they play a key role in regulating complex biological processes, including offspring development and mother–offspring interactions. There are several competing theories attempting to explain the evolutionary origin of this monoallelic pattern of gene expression, but a prevailing view has emerged that holds that genomic imprinting is a consequence of conflict between maternal and paternal gene copies over maternal investment. However, many imprinting patterns and the apparent overabundance of maternally expressed genes remain unexplained and may be incompatible with current theory. Here we demonstrate that sole expression of maternal gene copies is favored by natural selection because it increases the adaptive integration of offspring and maternal genomes, leading to higher offspring fitness. This novel coadaptation theory for the evolution of genomic imprinting is consistent with results of recent studies on epigenetic effects, and it provides a testable hypothesis for the origin of previously unexplained major imprinting patterns across different taxa. In conjunction with existing hypotheses, our results suggest that imprinting may have evolved due to different selective pressures at different loci.     

Gene interactions in the evolution of genomic imprinting

Numerous evolutionary theories have been developed to explain the epigenetic phenomenon of genomic imprinting. Here, we explore a subset of theories wherein non-additive genetic interactions can favour imprinting. In the simplest genic interaction—the case of underdominance—imprinting can be favoured to hide effectively low-fitness heterozygous genotypes; however, as there is no asymmetry between maternally and paternally inherited alleles in this model, other means of enforcing monoallelic expression may be more plausible evolutionary outcomes than genomic imprinting. By contrast, more successful interaction models of imprinting rely on an asymmetry between the maternally and paternally inherited alleles at a locus that favours the silencing of one allele as a means of coordinating the expression of high-fitness allelic combinations. For example, with interactions between autosomal loci, imprinting functionally preserves high-fitness genotypes that were favoured by selection in the previous generation. In this scenario, once a focal locus becomes imprinted, selection at interacting loci favours a matching imprint. Uniparental transmission generates similar asymmetries for sex chromosomes and cytoplasmic factors interacting with autosomal loci, with selection favouring the expression of either maternal or paternally derived autosomal alleles depending on the pattern of transmission of the uniparentally inherited factor. In a final class of models, asymmetries arise when genes expressed in offspring interact with genes expressed in one of its parents. Under such a scenario, a locus evolves to have imprinted expression in offspring to coordinate the interaction with its parent''s genome. We illustrate these models and explore key links and differences using a unified framework.     

Accelerated evolution of sex chromosomes in aphids, an x0 system

Sex chromosomes play a role in many important biological processes, including sex determination, genomic conflicts, imprinting, and speciation. In particular, they exhibit several unusual properties such as inheritance pattern, hemizygosity, and reduced recombination, which influence their response to evolutionary factors (e.g., drift, selection, and demography). Here, we examine the evolutionary forces driving X chromosome evolution in aphids, an XO system where females are homozygous (XX) and males are hemizygous (X0) at sex chromosomes. We show by simulations that the unusual mode of transmission of the X chromosome in aphids, coupled with cyclical parthenogenesis, results in similar effective population sizes and predicted levels of genetic diversity for X chromosomes and autosomes under neutral evolution. These results contrast with expectations from standard XX/XY or XX/X0 systems (where the effective population size of the X is three-fourths that of autosomes) and have deep consequences for aphid X chromosome evolution. We then localized 52 microsatellite markers on the X and 351 on autosomes. We genotyped 167 individuals with 356 of these loci and found similar levels of allelic richness on the X and on the autosomes, as predicted by our simulations. In contrast, we detected higher dN and dN/dS ratio for X-linked genes compared with autosomal genes, a pattern compatible with either positive or relaxed selection. Given that both types of chromosomes have similar effective population sizes and that the single copy of the X chromosome of male aphids exposes its recessive genes to selection, some degree of positive selection seems to best explain the higher rates of evolution of X-linked genes. Overall, this study highlights the particular relevance of aphids to study the evolutionary factors driving sex chromosomes and genome evolution.     

Does Breeding Ornamentation Signal Genetic Quality in Arctic charr, <Emphasis Type="Italic">Salvelinus alpinus</Emphasis>?

Genetic theories of sexual selection predict that most ornamental secondary sexual traits provide reliable indication of the genetic quality of their bearers. Accordingly, also the offspring of mates with elaborate mating display should perform better than those of less conspicuous counterparts. In this study, we used Arctic charr (Salvelinus alpinus) as a model species to investigate whether the variation in a carotenoid-based red breeding coloration (a sexually dichromatic trait) in different sexes would reflect differences in individual genetic variability, one measure of individual quality, and/or indirectly, be manifested in variation in the offspring’s early viability and growth. We created maternal half-sibling families by artificially fertilizing the eggs with milt from bright- and pale-coloured males and then held the resulting progenies under identical hatchery conditions. The expression of red coloration among parental fish was not associated with their genetic diversity estimates in either sex nor did offspring sired by bright males consistently differ in terms of embryo survival or endogenous growth efficiency from offspring sired by pale males. By contrast, maternal effects were notably strong and, additionally, the degree of female coloration was negatively linked to their reproductive potential. The more intensely coloured females had a smaller relative fecundity and they also produced offspring of lower viability, implying a significant trade-off in resource allocation between ornamentation and offspring. Our results indicate that the red breeding ornamentation of Arctic charr is likely to be informative rather among females than males when the reproductive quality is predicted on grounds of the number of offspring produced. Nevertheless, this study does not support the direct selection hypothesis in explaining the evolution of female ornamentation, but rather suggests that the less intense coloration of female charr compared to males may reflect inter-sexual differences in the trade-off between natural and sexual selection.     

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.     

Maternal investment and male reproductive success in angiosperms: parent-offspring conflict or sexual selection?

It is possible to interpret components of seed development in angiosperms from the perspective of parent-offspring conflict (a special case of kin selection) or sexual selection. Available parent-offspring conflict models predict the evolution of traits determining the outcome of competition among related individuals soliciting maternal resources. In such models, ‘selfishness’ may spread even if it reduces female fecundity and thus population mean fitness may decline. These models are limited, however, because most of them do not simultaneously consider selection among maternal genotypes varying in the tendency to respond to their offspring. Available sexual selection models, in contrast, do consider the joint evolution of polygenic male traits (influencing viability, mating success and fecundity) and female preferences (influencing the mating success of different male phenotypes). These models have shown that male traits may evolve that are non-optimal with respect to viability. Only one recent sexual selection model explicitly incorporates direct fecundity selection upon females; this model concludes that fecundity will be maximized at equilibrium. Hence population mean fitness may decline due to reduced male viability but not due to diminished female fecundity. Available sexual selection models, however, are limited because they do not consider the effects of interactions among relatives. The assumptions and qualitative results of the two types of models are compared and discussed in the context of seed development. Differential allocation of maternal resources among genetically distinct developing seeds may be viewed from the perspective of either. Because the results of the available models of parent-offspring conflict and sexual selection are not wholly consistent and because data confirming the genetic basis of maternal patterns of investment or differential male reproductive success are scant, it is not clear which set of conclusions is most appropriate to apply to plants. To achieve the generality towards which mathematical approaches aspire, new models concerning the evolution of traits influencing resource allocation in plants must incorporate the components of both parent-offspring conflict and sexual selection.     

Conflict theory of genomic imprinting in mammals

In mammals, some embryonic genes are expressed differently depending on whether they are inherited from the sperm or egg, a phenomenon known as genomic imprinting. The information on the parental origin is transmitted by an epigenetic mark. Both the molecular mechanisms and evolutionary processes of genomic imprinting have been studied extensively. Here, I illustrate the simplest evolutionary dynamics of imprinting evolution based on the “conflict theory,” by considering the evolution of a gene encoding an embryonic growth factor controlling the maternal resource supply. It demonstrates that (a) the autosomal genes controlling placenta development to modify maternal resource acquisition may evolve a strong asymmetry of gene expression, provided the mother has some chance of accepting multiple males. (b) The genomic imprinting may not evolve if there is a small fraction of recessive deleterious mutations on the gene. (c) The growth-enhancing genes should evolve to paternally expressed, while the growth-suppressing genes should evolve to maternally expressed. (d) The X-linked genes also evolve genomic imprinting, but the main evolutionary force is the sex difference in the optimal embryonic size. I discuss other aberrations that can be explained by the modified versions of the basic model.     

When fecundity does not equal fitness: evidence of an offspring quantity versus quality trade-off in pre-industrial humans

Maternal fitness should be maximized by the optimal division of reproductive investment between offspring number and offspring quality. While evidence for this is abundant in many taxa, there have been fewer tests in mammals, and in particular, humans. We used a dataset of humans spanning three generations from pre-industrial Finland to test how increases in maternal fecundity affect offspring quality and maternal fitness in contrasting socio-economic conditions. For 'resource-poor' landless families, but not 'resource-rich' landowning families, maternal fitness returns diminished with increased maternal fecundity. This was because the average offspring contribution to maternal fitness declined with increased maternal fecundity for landless but not landowning families. This decline was due to reduced offspring recruitment with increased maternal fecundity. However, in landowning families, recruited offspring fecundity increased with increased maternal fecundity. This suggests that despite decreased offspring recruitment, maternal fitness is not reduced in favourable socio-economic conditions due to an increase in subsequent offspring fecundity. These results provide evidence consistent with an offspring quantity-quality trade-off in the lifetime reproduction of humans from poor socio-economic conditions. The results also highlight the importance of measuring offspring quality across their whole lifespan to estimate reliably the fitness consequences of increased maternal fecundity.     

The adaptive value of stress-induced phenotypes: effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness

The question of why maternal stress influences offspring phenotype is of significant interest to evolutionary physiologists. Although embryonic exposure to maternally derived glucocorticoids (i.e., corticosterone) generally reduces offspring quality, effects may adaptively match maternal quality with offspring demand. We present results from an interannual field experiment in European starlings (Sturnus vulgaris) designed explicitly to examine the fitness consequences of exposing offspring to maternally derived stress hormones. We combined a manipulation of yolk corticosterone (yolk injections) with a manipulation of maternal chick-rearing ability (feather clipping of mothers) to quantify the adaptive value of corticosterone-induced offspring phenotypes in relation to maternal quality. We then examined how corticosterone-induced "matching" within this current reproductive attempt affected future fecundity and maternal survival. First, our results provide support that low-quality mothers transferring elevated corticosterone to eggs invest in daughters as predicted by sex allocation theory. Second, corticosterone-mediated sex-biased investment resulted in rapid male-biased mortality resulting in brood reduction, which provided a better match between maternal quality and brood demand. Third, corticosterone-mediated matching reduced investment in current reproduction for low-quality mothers, resulting in fitness gains through increased survival and future fecundity. Results indicate that the transfer of stress hormones to eggs by low-quality mothers can be adaptive since corticosterone-mediated sex-biased investment matches the quality of a mother to offspring demand, ultimately increasing maternal fitness. Our results also indicate that the branding of the proximate effects of maternal glucocorticoids on offspring as negative ignores the possibility that short-term phenotypic changes may actually increase maternal fitness.     

Sex specific X chromosome expression caused by genomic imprinting

The conflict theory of genomic imprinting predicts that imprinted genes are growth enhancing when paternally expressed and growth suppressing when maternally expressed. The expression pattern of autosomal imprinted genes generally fits these predictions. However, the conflict theory cannot easily account for the pattern of X-linked imprinting in humans and mice. This has led us to propose a novel hypothesis that X-linked imprinting has evolved to control sex specific gene expression in early embryos. The hypothesis links paternal X-imprinting (i.e. paternal copy silencing) to random X-inactivation and the retention of Y-linked copies, and links maternal X-imprinting to escape from random X-inactivation and the loss of Y-linked copies.The hypothesis offers a good explanation of the existing data on X-imprinted genes.     

ESS gene expression of X-linked imprinted genes subject to sexual selection

We define ESS (Evolutionary Stable Strategy) conditions for the evolution of genomic imprinting at an X-linked locus. The system analysed is designed for mammalian imprinting in which X-linked genes typically undergo random X-inactivation and lack Y-linked homologues. We consider two models that map cellular gene expression to fitness in females subject to random X-inactivation. In the first model, female fitness is simply a function of the average gene expression across all cells. In the second model, each cell contributes independently to fitness, and female fitness is assessed as the average of these contributions across all cells. In both models, imprinting readily evolves when sexual selection favours different levels of gene expression in the two sexes. Imprinting is beneficial as it improves adaptation in both sexes. There are limits to the improvement in adaptation when sexual selection is strong and favours greater gene expression in males (the heterogametic sex). We also consider the consequences of an active Y-linked homologue on the evolution of imprinting. Our analysis suggests that restrictive conditions apply for the evolution of polymorphic ESSs at an X-linked imprinted loci.     

Allometric scaling of the elevation of maternal energy intake during lactation

The amount of resources provided by the mother before birth has important and long-lasting effects on offspring fitness. Despite this, there is a large amount of variation in maternal investment seen in natural populations. Life-history theory predicts that this variation is maintained through a trade-off between the benefits of high maternal investment for the offspring and the costs of high investment for the mother. However, the proximate mechanisms underlying these costs of reproduction are not well understood. Here we used artificial selection for high and low maternal egg investment in a precocial bird, the Japanese quail (Coturnix japonica) to quantify costs of maternal reproductive investment. We show that females from the high maternal investment lines had significantly larger reproductive organs, which explained their overall larger body mass, and resulted in a higher resting metabolic rate (RMR). Contrary to our expectations, this increase in metabolic activity did not lead to a higher level of oxidative damage. This study is the first to provide experimental evidence for metabolic costs of increased per offspring investment.     

You are what your mother eats: evidence for maternal preconception diet influencing foetal sex in humans

Facultative adjustment of sex ratios by mothers occurs in some animals, and has been linked to resource availability. In mammals, the search for consistent patterns is complicated by variations in mating systems, social hierarchies and litter sizes. Humans have low fecundity, high maternal investment and a potentially high differential between the numbers of offspring produced by sons and daughters: these conditions should favour the evolution of facultative sex ratio variation. Yet little is known of natural mechanisms of sex allocation in humans. Here, using data from 740 British women who were unaware of their foetus's gender, we show that foetal sex is associated with maternal diet at conception. Fifty six per cent of women in the highest third of preconceptional energy intake bore boys, compared with 45% in the lowest third. Intakes during pregnancy were not associated with sex, suggesting that the foetus does not manipulate maternal diet. Our results support hypotheses predicting investment in costly male offspring when resources are plentiful. Dietary changes may therefore explain the falling proportion of male births in industrialized countries. The results are relevant to the current debate about the artificial selection of offspring sex in fertility treatment and commercial 'gender clinics'.     

Prenatal developmental conditions have long-term effects on offspring fecundity

Maternal effects, in which differences in parental state cause differences in offspring fitness, are important in trade-offs influencing an individual's optimal reproductive strategy. In zebra finches (Taeniopygia guttata) we manipulated the nutritional state for four weeks before the start of breeding through protein supplementation. Zebra finches were kept on identical diets during the rest of the experiment. We then tested the effects of maternal state on offspring size, survival and fecundity. In order to separate the effects of maternal state occurring through egg production, incubation and chick-rearing, we used a cross-fostering experiment. We show that a protein-rich diet prior to laying improved maternal body weight prior to breeding compared with birds on a protein-poor diet. Poorer maternal state prior to breeding gave rise to offspring with lower fecundity than offspring from birds in a better nutritional state. Maternal state is thought to affect the conditions developing offspring experience through the bird's ability to produce and incubate eggs. Male and female embryos differed in their responses to conditions at different developmental stages. This shows that embryonic developmental conditions and sex differences in vulnerability to these conditions need to be incorporated into future models of selection, life-history evolution and sex-ratio theory.