Adaptive Maternal Effects Shape Offspring Phenotype and Survival in Natal Environments.

AbstractMaternal effects can give newborns a head start in life by adjusting natal phenotypes to natal environments, yet their strength and adaptiveness are often difficult to investigate in natural populations. Here, we studied anticipatory maternal effects and their adaptiveness in common lizards in a seminatural experimental system. Specifically, we investigated how maternal environments (i.e., vegetation cover) and maternal phenotype (i.e., activity levels and body length) can shape offspring phenotype. We further studied whether such maternal effects influenced offspring survival in natal environments varying with respect to vegetation cover, conspecific density, and, consequently, maternal fitness. More active females from dense vegetation habitats produced bigger offspring than their less active counterparts, the contrary being true for sparse vegetation habitats. Moreover, females from dense vegetation habitats produced more active offspring and more active offspring survived better in dense vegetation habitats, resulting in greater maternal fitness through maternal effects. These results suggest adaptive anticipatory maternal effects, induced by vegetation structure and mediated by activity levels that may shape early-life prospects in natal environments.

Low repeatability of aversive learning in zebrafish (Danio rerio).

Aversive learning - avoiding certain situations based on negative experiences - can profoundly increase fitness in animal species, yet no studies have systematically quantified its repeatability. Therefore, we assessed the repeatability of aversive learning by conditioning approximately 100 zebrafish (Danio rerio) to avoid a colour cue associated with a mild electric shock. Across eight different colour conditions, zebrafish did not show consistent individual differences in aversive learning (R=0.04). Within conditions, when zebrafish were conditioned to the same colour, blue conditioning was more repeatable than green conditioning (R=0.15 and R=0.02). Overall, aversive learning responses of zebrafish were weak and variable. We speculate that the effect of aversive learning might have been too weak to quantify consistent individual differences, or directional selection might have eroded additive genetic variance. We also discuss how confounded repeatability assays and publication bias could have inflated estimates of repeatability in the literature.

Haploid selection within a single ejaculate increases offspring fitness.

An inescapable consequence of sex in eukaryotes is the evolution of a biphasic life cycle with alternating diploid and haploid phases. The occurrence of selection during the haploid phase can have far-reaching consequences for fundamental evolutionary processes including the rate of adaptation, the extent of inbreeding depression, and the load of deleterious mutations, as well as for applied research into fertilization technology. Although haploid selection is well established in plants, current dogma assumes that in animals, intact fertile sperm within a single ejaculate are equivalent at siring viable offspring. Using the zebrafish Danio rerio, we show that selection on phenotypic variation among intact fertile sperm within an ejaculate affects offspring fitness. Longer-lived sperm sired embryos with increased survival and a reduced number of apoptotic cells, and adult male offspring exhibited higher fitness. The effect on embryo viability was carried over into the second generation without further selection and was equally strong in both sexes. Sperm pools selected by motile phenotypes differed genetically at numerous sites throughout the genome. Our findings clearly link within-ejaculate variation in sperm phenotype to offspring fitness and sperm genotype in a vertebrate and have major implications for adaptive evolution.

Costs and benefits of giant sperm and sperm storage organs in Drosophila melanogaster.

In Drosophila, long sperm are favoured in sperm competition based on the length of the female's primary sperm storage organ, the seminal receptacle (SR). This sperm-SR interaction, together with a genetic correlation between the traits, suggests that the coevolution of exaggerated sperm and SR lengths may be driven by Fisherian runaway selection. Here, we explore the costs and benefits of long sperm and SR genotypes, both in the sex that carries them and in the sex that does not. We measured male and female fitness in inbred lines of Drosophila melanogaster derived from four populations previously selected for long sperm, short sperm, long SRs or short SRs. We specifically asked: What are the costs and benefits of long sperm in males and long SRs in females? Furthermore, do genotypes that generate long sperm in males or long SRs in females impose a fitness cost on the opposite sex? Answers to these questions will address whether long sperm are an honest indicator of male fitness, male post-copulatory success is associated with male precopulatory success, female choice benefits females or is costly, and intragenomic conflict could influence evolution of these traits. We found that both sexes have increased longevity in long sperm and long SR genotypes. Males, but not females, from long SR lines had higher fecundity. Our results suggest that sperm-SR coevolution is facilitated by both increased viability and indirect benefits of long sperm and SRs in both sexes.

Transgenerational effects of maternal sexual interactions in seed beetles.

Mating often bears large costs to females, especially in species with high levels of sexual conflict over mating rates. Given the direct costs to females associated with multiple mating, which include reductions in lifespan and lifetime reproductive success, past research focused on identifying potential indirect benefits (through increases in offspring fitness) that females may accrue. Far less attention has, however, been devoted to understanding how costs of sexual interactions to females may extend across generations. Hence, little is known about the transgenerational implications of variation in mating rates, or the net consequences of maternal sexual activities across generations. Using the seed beetle, Callosobruchus maculatus, a model system for the study of sexual conflict, we investigate the effects of mating with multiple males versus a single male, and tease apart effects due to sexual harassment and those due to mating per se, over three generations. A multigenerational analysis indicated that females that were exposed to ongoing sexual harassment and who also were permitted to mate with multiple males showed no difference in net fitness compared to females that mated just once without ongoing harassment. Intriguingly, however, females that were continually harassed, but permitted to mate just once, suffered a severe decline in net fitness compared to females that were singly (not harassed) or multiply mated (harassed, but potentially gaining benefits via mating with multiple males). Overall, the enhanced fitness in multiply mated compared to harassed females may indicate that multiple mating confers transgenerational benefits. These benefits may counteract, but do not exceed (i.e., we found no difference between singly and multiply mated females), the large transgenerational costs of harassment. Our study highlights the importance of examining transgenerational effects from an inclusive (looking at both indirect benefits but also costs) perspective, and the need to investigate transgenerational effects across several generations if we are to fully understand the consequences of sexual interactions, sexual conflict evolution, and the interplay of sexual conflict and multi-generational costs and benefits.

Paternal personality and social status influence offspring activity in zebrafish.

BACKGROUND: Evidence for the transmission of non-genetic information from father to offspring is rapidly accumulating. While the impact of chemical and physical factors such as toxins or diet on the fitness of the parents and their offspring have been studied extensively, the importance of behavioural and social circumstances has only recently been recognised. Behavioural traits such as personality characteristics can be relatively stable, and partly comprise a genetic component but we know little about the non-genetic transmission of plastic behavioural traits from parents to offspring. We investigated the relative effect of personality and of social dominance as indicators at the opposite ends of the plasticity range on offspring behaviour in the zebrafish (Danio rerio). We assessed male boldness, a behavioural trait that has previously been shown previously to possess genetic underpinnings, and experimentally manipulated male social status to assess the association between the two types of behaviour and their correlation with offspring activity. RESULTS: We found a clear interaction between the relatively stable and putative genetic effects based on inherited differences in personality and the experimentally induced epigenetic effects from changes in the social status of the father on offspring activity. CONCLUSIONS: Our study shows that offspring behaviour is determined by a combination of paternal personality traits and on-genetic effects derived from the social status of the father.

Paternal diet affects differential gene expression, but not sperm competition, in sons.

Parental environment can widely influence offspring phenotype, but paternal effects in the absence of parental care remain poorly understood. We asked if protein content in the larval diet of fathers affected paternity success and gene expression in their sons. We found that males reared on high-protein diet had sons that fared better during sperm competition, suggesting that postcopulatory sexual selection is subject to transgenerational paternal effects. Moreover, immune response genes were downregulated in sons of low-protein fathers, while genes involved in metabolic and reproductive processes were upregulated.

Evolution under dietary restriction increases male reproductive performance without survival cost.

Dietary restriction (DR), a reduction in nutrient intake without malnutrition, is the most reproducible way to extend lifespan in a wide range of organisms across the tree of life, yet the evolutionary underpinnings of the DR effect on lifespan are still widely debated. The leading theory suggests that this effect is adaptive and results from reallocation of resources from reproduction to somatic maintenance, in order to survive periods of famine in nature. However, such response would cease to be adaptive when DR is chronic and animals are selected to allocate more resources to reproduction. Nevertheless, chronic DR can also increase the strength of selection resulting in the evolution of more robust genotypes. We evolved Drosophila melanogaster fruit flies on 'DR', 'standard' and 'high' adult diets in replicate populations with overlapping generations. After approximately 25 generations of experimental evolution, male 'DR' flies had higher fitness than males from 'standard' and 'high' populations. Strikingly, this increase in reproductive success did not come at a cost to survival. Our results suggest that sustained DR selects for more robust male genotypes that are overall better in converting resources into energy, which they allocate mostly to reproduction.

The Metatron: an experimental system to study dispersal and metaecosystems for terrestrial organisms.

Dispersal of organisms generates gene flow between populations. Identifying factors that influence dispersal will help predict how species will cope with rapid environmental change. We developed an innovative infrastructure, the Metatron, composed of 48 interconnected patches, designed for the study of terrestrial organism movement as a model for dispersal. Corridors between patches can be flexibly open or closed. Temperature, humidity and illuminance can be independently controlled within each patch. The modularity and adaptability of the Metatron provide the opportunity for robust experimental design for the study of 'meta-systems'. We describe a pilot experiment on populations of the butterfly Pieris brassicae and the lizard Zootoca vivipara in the Metatron. Both species survived and showed both disperser and resident phenotypes. The Metatron offers the opportunity to test theoretical models in spatial ecology.

Short-term variation in sperm competition causes sperm-mediated epigenetic effects on early offspring performance in the zebrafish.

The inheritance of non-genetic factors is increasingly seen to play a major role in ecology and evolution. While the causes and consequences of epigenetic effects transmitted from the mother to the offspring have received ample attention, much less is known about how variation in the condition of the father affects the offspring. Here, we manipulated the intensity of sperm competition experienced by male zebrafish Danio rerio to investigate the potential for sperm-mediated epigenetic effects over a relatively short period of time. We found that the rapid responses of males to varying intensity of sperm competition not only affected sperm traits as shown previously, but also the performance of the resulting offspring. We observed that males exposed to high intensity of sperm competition produced faster swimming and more motile sperm, and sired offspring that hatched over a narrower time frame but exhibited a lower survival rate than males exposed to low intensity of sperm competition. Our results provide striking evidence for short-term paternal effects and the possible fitness consequences of such sperm-mediated non-genetic factors not only for the resulting offspring but also for the female.

The importance of habitat resistance for movement decisions in the common lizard, Lacerta vivipara.

BACKGROUND: Movement behaviour can be influenced by a multitude of biotic and abiotic factors. Here, we investigate the speed of movement in relation to environmental and individual phenotypic properties in subadult common lizards (Lacerta vivipara). We aim to disentangle the importance of substrate, cover, humidity, basking opportunity and individual phenotype on moving tendencies in 12 treatment combinations, at which each lizard was tested. RESULTS: We find that movement behaviour depends on the starting conditions, the physical properties of the dispersal corridor, and on the individuals' phenotype. Specifically, the presence of cover and substrate providing suitable traction in the corridor had positive effects on individual movement decisions. Additionally, we find high phenotypic variation in the propensity to move dependent on the presence of cover. Individual back patterns also strongly affected movement decisions in interaction with the physical properties of the dispersal corridor. CONCLUSIONS: Our results highlight the importance of understanding the habitat resistance for movement patterns, with humid habitats with covering vegetation providing the best conditions to initiate movement in the common lizard. In addition, population effects, differences in back pattern phenotype and individual plasticity were identified as key parameters influencing movement behaviour.

Sex differences in allometry for phenotypic traits in mice indicate that females are not scaled males.

Sex differences in the lifetime risk and expression of disease are well-known. Preclinical research targeted at improving treatment, increasing health span, and reducing the financial burden of health care, has mostly been conducted on male animals and cells. The extent to which sex differences in phenotypic traits are explained by sex differences in body weight remains unclear. We quantify sex differences in the allometric relationship between trait value and body weight for 363 phenotypic traits in male and female mice, recorded in >2 million measurements from the International Mouse Phenotyping Consortium. We find sex differences in allometric parameters (slope, intercept, residual SD) are common (73% traits). Body weight differences do not explain all sex differences in trait values but scaling by weight may be useful for some traits. Our results show sex differences in phenotypic traits are trait-specific, promoting case-specific approaches to drug dosage scaled by body weight in mice.

Intergenerational effects of overfeeding on aversive learning in zebrafish (Danio rerio).

The obesity epidemic is concerning as obesity appears to negatively impact cognition and behavior. Furthermore, some studies suggest that this negative effect could be carried across generations from both mothers and fathers although evidence is not consistent. Here, we attempt to address how obesogenic diets in the parental generation (F0) can impact offspring's cognition and anxiety intergenerationally (F1) in a zebrafish model. We compare both mean trait values and their variances. Using a multifactorial design, we created a total of four groups: F1T (treatment mothers × treatment fathers); F1M (treatment mothers × control fathers); F1P (treatment fathers × control mothers); and F1C (control mothers × control fathers, F1C); and subjected them to anxiety tank tests and aversive learning assays. When both parents were exposed, offspring (F1T) displayed the poorest aversive learning, while offspring that only had one parent exposed (F1P and F1M) learnt the aversive learning task the best. Zebrafish in all groups displayed no statistically significant differences in anxiety-associated behaviors. Males and females also performed similarly in both anxiety and aversive learning assays. While all F1 groups had similar levels of fasting blood glucose, variance in glucose levels were reduced in F1P and F1T indicating the importance of investigating heteroskedasticity between groups. Furthermore, anxiety behaviors of these two groups appeared to be less repeatable. To our knowledge, this is the first study to test the intergenerational effects of an obesogenic diet on zebrafish cognition. Our multifactorial design as well as repeated tests also allowed us to disentangle maternal and paternal effects (as well as combined effects) and accurately detect subtle information such as between-individual variation.

The effects of an obesogenic diet on behavior and cognition in zebrafish (Danio rerio): Trait average, variability, repeatability, and behavioral syndromes.

The obesity epidemic, largely driven by the accessibility of ultra-processed high-energy foods, is one of the most pressing public health challenges of the 21st century. Consequently, there is increasing concern about the impacts of diet-induced obesity on behavior and cognition. While research on this matter continues, to date, no study has explicitly investigated the effect of obesogenic diet on variance and covariance (correlation) in behavioral traits. Here, we examined how an obesogenic versus control diet impacts means and (co-)variances of traits associated with body condition, behavior, and cognition in a laboratory population of ~160 adult zebrafish (Danio rerio). Overall, an obesogenic diet increased variation in several zebrafish traits. Zebrafish on an obesogenic diet were significantly heavier and displayed higher body weight variability; fasting blood glucose levels were similar between control and treatment zebrafish. During behavioral assays, zebrafish on the obesogenic diet displayed more exploratory behavior and were less reactive to video stimuli with conspecifics during a personality test, but these significant differences were sex-specific. Zebrafish on an obesogenic diet also displayed repeatable responses in aversive learning tests whereas control zebrafish did not, suggesting an obesogenic diet resulted in more consistent, yet impaired, behavioral responses. Where behavioral syndromes existed (inter-class correlations between personality traits), they did not differ between obesogenic and control zebrafish groups. By integrating a multifaceted, holistic approach that incorporates components of (co-)variances, future studies will greatly benefit by quantifying neglected dimensions of obesogenic diets on behavioral changes.

An efficient new assay for measuring zebrafish anxiety: Tall tanks that better characterize between-individual differences.

BACKGROUND: Zebrafish (Danio rerio) are increasingly being used to model anxiety. A common behavioral assay employed for assessing anxiety-like behaviors in zebrafish is the "novel tank test". We hypothesized that using deeper tanks in this test would result in greater between-individual variation in behavioral responses and a more 'repeatable' assay. NEW METHODS: After mapping the literature and identifying common behavioral parameters used in analysis, we performed novel tank anxiety tests in both custom-designed 'tall' tanks with increased depth and 'short' trapezoidal tanks. We compared the repeatability of the behavioral parameters between tall and short tanks and also investigated sex differences. RESULTS: Overall, regardless of tank depth, almost all behavioral parameters associated with anxiety in zebrafish were significantly repeatable (R = 0.24 to 0.60). Importantly, our tall tanks better captured between-individual differences, resulting in higher repeatability estimates (average repeatability tall tanks: R = 0.46; average repeatability short tanks: R = 0.36) and clearer sex differences. CONCLUSIONS: Our assay using tall tanks has advantages over tests based on short tanks which underestimate repeatability. We argue that use of deeper tanks will improve the reliability of behavioral data across studies using novel tank tests for zebrafish. Our results also call for increased attention in designing the most appropriate assay in biomedical and behavioral sciences as current methods may lack the sensitivity to detect subtle, yet important, information, such as between-individual variation, an important component in assessing the reliability of behavioral data.

Sexual dimorphism in trait variability and its eco-evolutionary and statistical implications.

Biomedical and clinical sciences are experiencing a renewed interest in the fact that males and females differ in many anatomic, physiological, and behavioural traits. Sex differences in trait variability, however, are yet to receive similar recognition. In medical science, mammalian females are assumed to have higher trait variability due to estrous cycles (the 'estrus-mediated variability hypothesis'); historically in biomedical research, females have been excluded for this reason. Contrastingly, evolutionary theory and associated data support the 'greater male variability hypothesis'. Here, we test these competing hypotheses in 218 traits measured in >26,900 mice, using meta-analysis methods. Neither hypothesis could universally explain patterns in trait variability. Sex bias in variability was trait-dependent. While greater male variability was found in morphological traits, females were much more variable in immunological traits. Sex-specific variability has eco-evolutionary ramifications, including sex-dependent responses to climate change, as well as statistical implications including power analysis considering sex difference in variance.

Males and females differ in appearance, physiology and behavior. But we do not fully understand the health and evolutionary consequences of these differences. One reason for this is that, until recently, females were often excluded from medical studies. This made it difficult to know if a treatment would perform as well in females as males. To correct this, organizations that fund research now require scientists to include both sexes in studies. This has led to some questions about how to account for sex differences in studies. One reason females have historically been excluded from medical studies is that some scientists assumed that they would have more variable responses to a particular treatment based on their estrous cycles. Other scientists, however, believe that males of a given species might be more variable because of the evolutionary pressures they face in competing for mates. Better understanding how males and females vary would help scientists better design studies to ensure they provide accurate answers. Now, Zajitschek et al. debunk both the idea that males are more variable and the idea that females are more variable. To do this, Zajitschek et al. analyzed differences in 218 traits, like body size or certain behaviors, among nearly 27,000 male and female mice. This showed that neither male mice nor female mice were universally more different from other mice of their sex across all features. Instead, sex differences in how much variation existed in male or female mice depended on the individual trait. For example, males varied more in physical features like size, while females showed more differences in their immune systems. The results suggest it is particularly important to consider sex-specific variability in both medical and other types of studies. To help other researchers better design experiments to factor in such variability, Zajitschek et al. created an interactive tool that will allow scientists to look at sex-based differences in individual features among male or female mice.

Demographic costs of inbreeding revealed by sex-specific genetic rescue effects.

BACKGROUND: Inbreeding can slow population growth and elevate extinction risk. A small number of unrelated immigrants to an inbred population can substantially reduce inbreeding and improve fitness, but little attention has been paid to the sex-specific effects of immigrants on such "genetic rescue". We conducted two subsequent experiments to investigate demographic consequences of inbreeding and genetic rescue in guppies. RESULTS: Populations established from pairs of full siblings that were descended either from two generations of full-sibling inbreeding or unrelated outbred guppies did not grow at different rates initially, but when the first generation offspring started breeding, outbred-founded populations grew more slowly than inbred-founded populations. In a second experiment, adding two outbred males to the inbred populations resulted in significantly faster population growth than in control populations where no immigrants were added. Adding females resulted in growth at a rate intermediate to the control and male-immigrant treatments. CONCLUSION: The slower growth of the outbred-founded than inbred-founded populations is the opposite of what would be expected under inbreeding depression unless many deleterious recessive alleles had already been selectively purged in the inbreeding that preceded the start of the experiment, and that significant inbreeding depression occurred when the first generation offspring in outbred-founded populations started to inbreed. The second experiment revealed strong inbreeding depression in the inbred founded populations, despite the apparent lack thereof in these populations earlier on. Moreover, the fact that the addition of male immigrants resulted in the highest levels of population growth suggests that sex-specific genetic rescue may occur in promiscuous species, with male rescue resulting in higher levels of outbreeding than female rescue.

Sexual dimorphism in life history: age, survival, and reproduction in male and female field crickets Teleogryllus commodus under seminatural conditions.

Males and females differ in their reproductive strategies. Accordingly, sexually dimorphic optima in the allocation of resources to reproduction should select for sex-specific life histories, including sex-specific resolution of the key trade-off between reproduction and longevity. While males are expected to increase reproductive effort with increasing age under sexual selection theory, female reproductive effort should rather decrease after maturity, due to waning selection pressure at older ages. Sex differences in reproductive trade-offs and in the external mortality hazards experienced during the population's evolutionary history are both likely to shape sex differences in reproductive and actuarial (age-specific mortality) aging. Despite the importance of small-bodied, short-lived animals as laboratory models for life-history and aging studies, very little is known about sex differences in life-history patterns under natural conditions. Here, we tested for sex-specific patterns of reproductive and actuarial aging in field crickets under near-natural conditions. Both males and females showed actuarial senescence, with females exhibiting more rapid aging than males but with a later onset. Female and male reproductive effort showed a senescent decrease, with the peaks at different ages. Our findings provide the first demonstration of sexual dimorphism in age-dependent patterns of both survival and reproduction in an insect under near-natural conditions.

Evolution Under Dietary Restriction Decouples Survival From Fecundity in Drosophila melanogaster Females.

One of the key tenets of life-history theory is that reproduction and survival are linked and that they trade-off with each other. When dietary resources are limited, reduced reproduction with a concomitant increase in survival is commonly observed. It is often hypothesized that this dietary restriction effect results from strategically reduced investment in reproduction in favor of somatic maintenance to survive starvation periods until resources become plentiful again. We used experimental evolution to test this "waiting-for-the-good-times" hypothesis, which predicts that selection under sustained dietary restriction will favor increased investment in reproduction at the cost of survival because "good-times" never come. We assayed fecundity and survival of female Drosophila melanogaster fruit flies that had evolved for 50 generations on three different diets varying in protein content-low (classic dietary restriction diet), standard, and high-in a full-factorial design. High-diet females evolved overall increased fecundity but showed reduced survival on low and standard diets. Low-diet females evolved reduced survival on low diet without corresponding increase in reproduction. In general, there was little correspondence between the evolution of survival and fecundity across all dietary regimes. Our results contradict the hypothesis that resource reallocation between fecundity and somatic maintenance underpins life span extension under dietary restriction.