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Data from: Accounting for genetic differences among unknown parents in microevolutionary studies: how to include genetic groups in quantitative genetic animal models

Quantifying and predicting microevolutionary responses to environmental change requires unbiased estimation of quantitative genetic parameters in wild populations. 'Animal models', which utilize pedigree data to separate genetic and environmental effects on phenotypes, provide powerful means to estimate key parameters and have revolutionized quantitative genetic analyses of wild populations. However, pedigrees collected in wild populations commonly contain many individuals with unknown parents. When unknown parents are non-randomly associated with genetic values for focal traits, animal model parameter estimates can be severely biased. Yet, such bias has not previously been highlighted and statistical methods designed to minimize such biases have not been implemented in evolutionary ecology. We first illustrate how the occurrence of non-random unknown parents in population pedigrees can substantially bias animal model predictions of breeding values and estimates of additive genetic variance, and create spurious temporal trends in predicted breeding values in the absence of local selection. We then introduce 'genetic group' methods, which were developed in agricultural science, and explain how these methods can minimize bias in quantitative genetic parameter estimates stemming from genetic heterogeneity among individuals with unknown parents. We summarize the conceptual foundations of genetic group animal models and provide extensive, step-by-step tutorials that demonstrate how to fit such models in a variety of software programs. Furthermore, we provide new functions in r that extend current software capabilities and provide a standardized approach across software programs to implement genetic group methods. Beyond simply alleviating bias, genetic group animal models can directly estimate new parameters pertaining to key biological processes. We discuss one such example, where genetic group methods potentially allow the microevolutionary consequences of local selection to be distinguished from effects of immigration and resulting gene flow. We highlight some remaining limitations of genetic group models and discuss opportunities for further development and application in evolutionary ecology. We suggest that genetic group methods should no longer be overlooked by evolutionary ecologists, but should become standard components of the toolkit for animal model analyses of wild population data sets.

Data from: Transcriptomes of parents identify parenting strategies and sexual conflict in a subsocial beetle

Parenting in the burying beetle Nicrophorus vespilloides is complex and, unusually, the sex and number of parents that can be present is flexible. Such flexibility is expected to involve specialized behaviour by the two sexes under biparental conditions. Here, we show that offspring fare equally well regardless of the sex or number of parents present. Comparing transcriptomes, we find a largely overlapping set of differentially expressed genes in both uniparental and biparental females and in uniparental males including vitellogenin, associated with reproduction, and takeout, influencing sex-specific mating and feeding behaviour. Gene expression in biparental males is similar to that in non-caring states. Thus, being 'biparental' in N. vespilloides describes the family social organization rather than the number of directly parenting individuals. There was no specialization; instead, in biparental families, direct male parental care appears to be limited with female behaviour unchanged. This should lead to strong sexual conflict.

opencc-zeroDec 2017View details →

Data from: Manipulation of parental nutritional condition reveals competition among family members

Parental care is thought to be costly, as it consumes time and energy. Such costs might be reduced in animal parents that raise their young on valuable food sources such as dung or carcasses, as parents are able to invest in self-maintenance by feeding from the same resource. However, this might lower the nutritional value for other family members and, as a consequence, food competition might arise. To promote our understanding of the outcome of such competition, we manipulated the necessity of parents to feed from the resource. Using a full factorial design, we paired food-deprived or well-fed males with food-deprived or well-fed females of burying beetles, which are known to raise their young on vertebrate cadavers. We found that food-deprived parents consumed more of the carrion than those that were well-fed and this had a negative impact on other family members. However, the outcome of the competition depended on the sex of the parents, with females suffering when males fed more and offspring suffering when females fed more. Thus, family life involves selfish elements, as both parents remove resources for the purpose of self-maintenance. However, females show altruistic aspects, as they appear to restrict their food consumption for the benefit of their offspring when paired with a food-deprived male. Interestingly, males extend their stay with the brood when having faced food scarcity prior to reproduction, presumably to replenish their energy reserves. Our study therefore reveals that breeding on shared resources can promote family living, but also results in competition.

Data from: Sex differences in parental care: gametic investment, sexual selection and social environment

Male and female parents often provide different type and amount of care to their offspring. Three major drivers have been proposed to explain parental sex roles: (i) differential gametic investment by males and females that precipitates into sex difference in care, (ii) different intensity of sexual selection acting on males and females, and (iii) biased social environment that facilitates the more common sex to provide more care. Here we provide the most comprehensive assessment of these hypotheses using detailed parental care data from 792 bird species covering 126 families. We found no evidence for the gametic investment hypothesis: neither gamete sizes nor gamete production by males relative to females was related to sex difference in parental care. However, sexual selection correlated with parental sex roles, because the male share in care relative to female decreased with both extra-pair paternity and frequency of polygamy. Parental sex roles were also related to social environment, because male parental care increased with male-biased adult sex ratios. Taken together, our results are consistent with recent theories suggesting that gametic investment is not tied to parental sex roles, and highlight the importance of both sexual selection and adult sex ratios in influencing parental sex roles.

Data from: Reduced fitness in progeny from old parents in a natural population

A nongenetic, transgenerational effect of parental age on offspring fitness has been described in many taxa in the laboratory. Such a transgenerational fitness effect will have important influences on population dynamics, population age structure, and the evolution of aging and lifespan. However, effects of parental age on offspring lifetime fitness have never been demonstrated in a natural population. We show that parental age has sex-specific negative effects on lifetime fitness, using data from a pedigreed insular population of wild house sparrows. Birds whose parents were older produced fewer recruits annually than birds with younger parents, and the reduced number of recruits translated into a lifetime fitness difference. Using a long-term cross-fostering experiment, we demonstrate that this parental age effect is unlikely to be the result of changes in the environment but that it potentially is epigenetically inherited. Our study reveals the hidden consequences of late-life reproduction that persist into the next generation.

Data from: A multigenerational effect of parental age on offspring size but not fitness in common duckweed (Lemna minor)

Classic theories on the evolution of senescence make the simplifying assumption that all offspring are of equal quality, so that demographic senescence only manifests through declining rates of survival or fecundity. However, there is now evidence that, in addition to declining rates of survival and fecundity, many organisms are subject to age-related declines in the quality of offspring produced (i.e. parental age effects). Recent modelling approaches allow for the incorporation of parental age effects into classic demographic analyses, assuming that such effects are limited to a single generation. Does this 'single-generation' assumption hold? To find out, we conducted a laboratory study with the aquatic plant Lemna minor, a species for which parental age effects have been demonstrated previously. We compared the size and fitness of 423 lab-cultured plants (asexually-derived ramets) representing various birth orders, and ancestral 'birth-order genealogies'. We found that offspring size and fitness both declined with increasing 'immediate' birth order (i.e. birth order with respect to the immediate parent), but only offspring size was affected by ancestral birth order. Thus, the assumption that parental age effects on offspring fitness are limited to a single generation does in fact hold for L. minor. This result will guide theorists aiming to refine and generalise modelling approaches that incorporate parental age effects into evolutionary theory on senescence.

Data from: Aposematism in the burying beetle? Dual function of anal fluid in parental care and chemical defense

Burying beetles (Nicrophorus vespilloides) bear distinctive and variable orange-black patterning on their elytra and produce an anal exudate from their abdomen when threatened. During breeding, the anal exudates contribute to the antimicrobial defense of the breeding resource. We investigated whether the anal exudates also provide a responsive chemical defense, which is advertised to potential avian predators by the beetle's orange and black elytral markings. We found that that the orange-black elytral markings of the burying beetle are highly conspicuous for avian predators against range of backgrounds, by using computer simulations. Using bioassays with wood ants, we also showed that the burying beetle's anal exudates are aversive to potential predators. From these results, and other evidence in the literature, we conclude that the evidence for aposematism in the burying beetle is as strong as the evidence for many other classically aposematic species, such as defended Hymenopterans, ladybirds, or poisonous frogs. Nevertheless, we also report unexpectedly high levels of individual variation in coloration and chemical defenses, as well as sex differences. We suggest that this variation might be partly due to conflicting selection pressures, particularly on the dual function of the exudates, and partly to nutritional differences in the developmental environment. The ecology of the burying beetles (Nicrophorus spp.) differs markedly from better-studied aposematic insects. This genus thus offers new potential for understanding the evolution of aposematism in general.

opencc-zeroDec 2011View details →

Data from: The costs of parental care: a meta-analysis of the trade-off between parental effort and survival in birds

A fundamental premise of life-history theory is that organisms that increase current reproductive investment suffer increased mortality. Possibly the most studied life-history phenotypic relationship is the trade-off between parental effort and survival. However, evidence supporting this trade-off is equivocal. Here, we conducted a meta-analysis to test the generality of this tenet. Using experimental studies that manipulated parental effort in birds we show that: 1) the effect of parental effort on survival was similar across species regardless of phylogeny, 2) individuals that experienced reduced parental effort had similar survival probabilities than control individuals, regardless of sex, and 3) males that experienced increased parental effort were less likely to survive than control males, whereas females that experienced increased effort were just as likely to survive as control females. Our results suggest that the trade-off between parental effort and survival is more complex than previously assumed. Finally, our study provides recommendations of unexplored avenues of future research into life-history trade-offs.

Data from: Flexibility in the duration of parental care: female leopards prioritise cub survival over reproductive output

1.Deciding when to terminate care of offspring is a key consideration for parents. Prolonging care may increase fitness of current offspring, but it can also reduce opportunities for future reproduction. Despite its evolutionary importance, few studies have explored the optimal duration of parental care, particularly among large carnivores. 2.We used a 40-year dataset to assess the trade-offs associated with the length of maternal care in leopards in the Sabi Sand Game Reserve, South Africa. We compared the costs imposed by care on the survival and residual reproductive value of leopard mothers against the benefits derived from maternal care in terms of increased offspring survival, recruitment and reproduction. We also examined the demographic and ecological factors affecting the duration of care in light of five explanatory hypotheses: litter-size, sex-allocation, resource-limitation, timing-of-independence, and terminal-investment. 3.Duration of care exhibited by female leopards varied markedly, from 9–35 months. Mothers did not appear to suffer any short- or long-term survival costs from caring for cubs, but extending care reduced the number of litters that mothers could produce during their lifetimes. Interestingly, the duration of care did not appear to affect the post-independence survival or reproductive success of offspring (although it may have indirectly affected offspring survival by influencing dispersal distance). However, results from generalised linear mixed models showed that mothers prolonged care during periods of prey scarcity, supporting the resource-limitation hypothesis. Female leopards also cared for sons longer than daughters, in line with the sex-allocation hypothesis. 4.Cub survival is an important determinant of the lifetime reproductive success in leopards. By buffering offspring against environmental perturbation without jeopardizing their own survivorship, female leopards apparently 'hedge their bets' with current offspring rather than gamble on future offspring which have a small probability of surviving. 5.In many species, parents put their own needs before that of their offspring. Leopard mothers appear sensitive to their offspring's demands, and adjust levels of care accordingly.

Data from: Within-family parent-offspring co-adaptation in a wild bird: on static traits, behavioural reaction norms and sex differences

Parental care, a central component of reproduction in a wide range of animal species, often involves elaborate behavioural interactions between parents and their offspring. Due to the reciprocal nature of these interactions, it has been hypothesized that parental and offspring behaviours (e.g. parental food provisioning and offspring begging) are not only target but also agent of selection. These traits are therefore expected to co-evolve, ultimately leading to co-adaptation of parent and offspring behaviours within families. However, empirical data on such parent-offspring co-adaptation are limited, particularly for wild populations. Furthermore, mean levels of behaviour (as measured in previous studies) may not adequately describe the dynamic nature of the reciprocal interplay between parents and their offspring, and instead rather the behavioural reaction norms for provisioning and begging may be co-adapted. We applied a large-scale cross-fostering study over 3 consecutive breeding seasons to investigate whether provisioning behaviour of wild blue tit (Cyanistes caeruleus) parents co-varies with the begging behaviour of their genetic, cross-fostered offspring. We simultaneously analysed parent and offspring behaviours, both as static traits (mean levels) and behavioural reaction norms (offspring begging as a function of food deprivation and parental provisioning as a function of short-term experimental changes in brood size). Neither maternal nor paternal provisioning rates co-varied with the begging intensity of their genetic offspring when analysed as mean levels of behaviour. However, the slopes of the reaction norms for provisioning and begging were negatively correlated between male, but not female, parents and their genetic offspring. Thus, fathers that change their provisioning rate strongly with brood size sire offspring whose level of begging only weakly increases with hunger, and vice versa. The observed co-variation suggests the existence of sex-specific optima for parent-offspring trait combinations. Thus, our study not only highlights the importance of a behavioural reaction norm approach when investigating parent-offspring interactions, but also stresses the relevance of considering parents as separate units, at least for biparental species.

Data from: Differential allocation revisited: when should mate quality affect parental investment?

Differential allocation (DA) is the adaptive adjustment of reproductive investment (up or down) according to partner quality. A lack of theoretical treatments has led to some confusion in the interpretation of DA in the empirical literature. We present a formal framework for DA that highlights the nature of reproductive benefits versus costs for females mated to males of different quality. Contrary to popular belief, analytical and stochastic dynamic models both show that additive benefits of male quality on offspring fitness have no effect on optimal levels of female investment and thus cannot produce DA. Instead, if offspring fitness is affected multiplicatively by male quality, or male quality affects the female cost function, DA is expected because of changes in the marginal benefits or costs of extra investment. Additive male quality effects on the female cost function can cause a novel form of weak DA, because reduced costs can slightly favor current over future reproduction. Combinations of these distinct effects in more realistic model scenarios can explain various patterns of positive and negative DA reported for different species and mating systems. Our model therefore sheds new light on the diversity of empirical results by providing a strong conceptual framework for the differential allocation hypothesis.

opencc-zeroDec 2012View details →

Data from: Environmental transmission of a personality trait: foster parent exploration behaviour predicts offspring exploration behaviour in zebra finches

Consistent behavioural differences among individuals are common in many species and can have important effects on offspring fitness. To understand such 'personality' variation, it is important to determine the mode of inheritance, but this has been quantified for only a few species. Here, we report results from a breeding experiment in captive zebra finches, Taeniopygia guttata, in which we cross-fostered offspring to disentangle the importance of genetic and non-genetic transmission of behaviour. Genetic and foster-parents' exploratory type was measured in a novel environment pre-breeding and offspring exploratory type was assessed at adulthood. Offspring exploratory type was predicted by the exploratory behaviour of the foster but not the genetic parents, whereas offspring size was predicted by genetic but not foster-parents' size. Other aspects of the social environment, such as rearing regime (uni- versus biparental), hatching position, brood size or an individual's sex did not influence offspring exploration. Our results therefore indicate that non-genetic transmission of behaviour can play an important role in shaping animal personality variation.

opencc-zeroMay 2020View details →

Data from: Effects of inbreeding on behavioural plasticity of parent-offspring interactions in a burying beetle

Inbreeding depression is defined as a fitness decline in progeny resulting from mating between related individuals, the severity of which may vary across environmental conditions. Such inbreeding-by-environment interactions might reflect that inbred individuals have a lower capacity for adjusting their phenotype to match different environmental conditions better, as shown in prior studies on developmental plasticity. Behavioural plasticity is more flexible than developmental plasticity because it is reversible and relatively quick, but little is known about its sensitivity to inbreeding. Here we investigate effects of inbreeding on behavioural plasticity in the context of parent-offspring interactions in the burying beetle Nicrophorus vespilloides. Larvae increase begging with the level of hunger, and parents increase their level of care when brood sizes increase. Here we find that inbreeding increased behavioural plasticity in larvae, reducing their time spent associating with a parent in response to the length of food-deprivation more than outbred larvae. However, inbreeding had no effect on the behavioural plasticity of offspring begging or any parental behaviour. Overall, our results show that inbreeding can increase behavioural plasticity. We suggest that inbreeding-by-environment interactions might arise when inbreeding is associated with too little or too much plasticity in response to changing environmental conditions.

opencc-zeroDec 2013View details →

Data from: Sexual size dimorphism is not associated with the evolution of parental care in frogs

Sex differences in parental care are thought to arise from differential selection on the sexes. Sexual dimorphism, including sexual size dimorphism (SSD), is often used as a proxy for sexual selection on males. Some studies have found an association between male-biased SSD (i.e., males larger than females) and the loss of paternal care. While the relationship between sexual selection on males and parental care evolution has been studied extensively, the relationship between female-biased SSD (i.e., females larger than males) and the evolution of parental care has received very little attention. Thus, we have little knowledge of whether female-biased SSD coevolves with parental care. In species displaying female-biased SSD, we might expect dimorphism to be associated with the evolution of paternal care or perhaps the loss of maternal care. Here, drawing on data for 99 extant frog species, we use comparative methods to evaluate how parental care and female-biased SSD have evolved over time. Generally, we find no significant correlation between the evolution of parental care and female-biased SSD in frogs. This suggests that differential selection on body size between the sexes is unlikely to have driven the evolution of parental care in these clades and questions whether we should expect sexual dimorphism to exhibit a general relationship with the evolution of sex differences in parental care.

Data from: Effects of offspring and parental inbreeding on parent-offspring communication

There is mounting evidence that inbreeding can have complex effects on social interactions among inbred and outbred individuals. Here, we investigate effects of offspring and maternal inbreeding on parent-offspring communication in the burying beetle Nicrophorus vespilloides. We find effects of the interaction between offspring and maternal inbreeding on maternal behavior. Outbred females provided more direct care towards inbred larvae, while inbred females provided similar levels of direct care towards inbred and outbred larvae. Furthermore, we find direct and indirect effects of offspring inbreeding on offspring begging and maternal behavior, respectively. Inbred larvae spent less time begging than outbred larvae, and (outbred) females provided more direct care and less indirect care towards inbred larvae. Finally, we find effects of the interaction between offspring and maternal inbreeding on larval body mass. Inbred and outbred offspring grew to a similar size when the female was outbred, whilst inbred offspring were smaller size when the female was inbred. Our results suggest that outbred females provided more care towards inbred offspring to compensate for their poor genetic quality. Our study advances our understanding of inbreeding by showing that inbreeding can have direct effects on the behavior of inbred individuals and indirect effects on the behavior of outbred individuals, and that indirect effects on outbred individuals, in turn, may influence the fitness of inbred individuals.

Data from: Morphological convergence between an allopolyploid and one of its parental species correlates with biased gene expression and DNA loss

The contribution of gene expression modulation to phenotypic evolution is of major importance to an understanding of the origin of divergent or convergent phenotypes during and following polyploid speciation. Here we analysed genome-wide gene expression in two subspecies of the allotetraploid species, Senecio mohavensis A. Gray, and its diploid parents S. flavus (Decne.) Sch. Bip. and S. glaucus L.. The tetraploid is morphologically much more similar to S. flavus, leading to earlier confusion over its taxonomic status. By means of an analysis of transcriptomes of all three species, we show that gene expression divergence between the parent species is relatively low (ca. 14% of loci), whereas there is significant unequal expression between ca. 20-25% of the parental homoeologues (gene copies) in the tetraploid. The majority of the expression bias in the tetraploid is in favour of S. flavus homoeologues (ca. 65% of the differentially expressed loci), and overall expression of this parental species sub-genome is higher than that of the S. glaucus sub-genome. To determine whether absence of expression of a particular S. glaucus homoeologue in the allotetraploid could be due to loss of DNA, we carried out a PCR-based assay and confirmed that in three out of 10 loci the S. glaucus homoeologue appeared absent. Our results suggest that biased gene expression is one cause of the allotetraploid S. mohavensis being more similar in morphology to one of its parent, S. flavus, and that such bias could result, in part, from loss of S. glaucus homoeologues at some loci in the allotetraploid.

Data from: Estimating parent-specific QTL effects through cumulating linked identity-by-state SNP effects in multiparental populations

The emergence of multiparental mapping populations enabled plant geneticists to gain deeper insights into the genetic architecture of major agronomic traits and to map quantitative trait loci (QTLs) controlling the expression of these traits. Although the investigated mapping populations are similar, one open question is whether genotype data should be modelled as identical by state (IBS) or identical by descent (IBD). Whereas IBS simply makes use of raw genotype scores to distinguish alleles, IBD data are derived from parental offspring information. We report on comparing IBS and IBD by applying two multiple regression models on four traits studied in the barley nested association mapping (NAM) population HEB-25. We observed that modelling parent-specific IBD genotypes produced a lower number of significant QTLs with increased prediction abilities compared with modelling IBS genotypes. However, at lower trait heritabilities the IBS model produced higher prediction abilities. We developed a method to estimate multiallelic QTL effects in multiparental populations from simple biallelic IBS data. This method is based on cumulating IBS-derived single-nucleotide polymorphism (SNP) effect estimates in a defined genetic region surrounding a QTL. Comparing the resulting parent-specific QTL effects with those obtained from IBD approaches revealed high accordance that could be confirmed through simulations. The method turned out to be also applicable to a barley multiparent advanced generation inter-cross (MAGIC) population. The 'cumulation method' represents a universal approach to differentiate parent-specific QTL effects in multiparental populations, even if no IBD information is available. In future, the method could further benefit from the availability of much denser SNP maps.

Data from: Parental effects alter the adaptive value of an adult behavioural trait

The parents' phenotype, or the environment they create for their young, can have long-lasting effects on their offspring, with profound evolutionary consequences. Yet virtually no work has considered how such parental effects might change the adaptive value of behavioural traits expressed by offspring upon reaching adulthood. To address this problem, we combined experiments on burying beetles (Nicrophorus vespilloides) with theoretical modelling, and focussed on one adult behavioural trait in particular: the supply of parental care. We manipulated the early life environment and measured the fitness payoffs associated with the supply of parental care when larvae reached maturity. We found that (1) adults that received low levels of care as larvae were less successful at raising larger broods, and suffered greater mortality as a result: they were low quality parents. Furthermore (2) high quality males that raised offspring with low quality females subsequently suffered greater mortality than brothers of equivalent quality, which reared larvae with higher quality females. Our analyses identify three general ways in which parental effects can change the adaptive value of an adult behavioural trait: by influencing the associated fitness benefits and costs; by consequently changing the evolutionary outcome of social interactions; and by modifying the evolutionarily stable expression of behavioural traits that are themselves parental effects.