The long-lasting legacy of reproduction: lifetime reproductive success shapes expected genetic contributions of humans after 10 generations.

An individual's lifetime reproductive success (LRS) measures its realized genetic contributions to the next generation, but how well does it predict this over longer periods? Here we use human genealogical data to estimate expected individual genetic contributions (IGC) and quantify the degree to which LRS, relative to other fitness proxies, predicts IGC over longer periods. This allows an identification of the life-history stages that are most important in shaping variation in IGC. We use historical genealogical data from two non-isolated local populations in Switzerland to estimate the stabilized IGC for 2230 individuals approximately 10 generations after they were born. We find that LRS explains 30% less variation in IGC than the best predictor of IGC, the number of grandoffspring. However, albeit less precise than the number of grandoffspring, we show that LRS does provide an unbiased prediction of IGC. Furthermore, it predicts IGC better than lifespan, and accounting for offspring survival to adulthood does not improve the explanatory power. Overall, our findings demonstrate the value of human genealogical data to evolutionary biology and suggest that reproduction-more than lifespan or offspring survival-impacts the long-term genetic contributions of historic humans, even in a population with appreciable migration.

The role of maternal age, growth, and environment in shaping offspring performance in an aerial conifer seed bank.

PREMISE: Maternal effects have been demonstrated to affect offspring performance in many organisms, and in plants, seeds are important mediators of these effects. Some woody plant species maintain long-lasting canopy seed banks as an adaptation to wildfires. Importantly, these seeds stored in serotinous cones are produced by the mother plant under varying ontogenetic and physiological conditions. METHODS: We sampled the canopy seed bank of a highly serotinous population of Pinus pinaster to test whether maternal age and growth and the environmental conditions during each crop year affected seed mass and ultimately germination and early survival. After determining retrospectively the year of each seed cohort, we followed germination and early survival in a semi-natural common garden. RESULTS: Seed mass was related to maternal age and growth at the time of seed production; i.e., slow-growing, older mothers had smaller seeds, and fast-growing, young mothers had larger seeds, which could be interpreted either as a proxy of senescence or as a maternal strategy. Seed mass had a positive effect on germination success, but aside from differences in seed mass, maternal age had a negative effect and diameter had a positive effect on germination timing and subsequent survival. CONCLUSIONS: The results highlight the importance of maternal conditions combined with seed mass in shaping seedling establishment. Our findings open new insights in the offspring performance deriving from long-term canopy seed banks, which may have high relevance for plant adaptation.

A comment on The adaptive value of gluttony: predators mediate the life history trade-offs of satiation threshold by Pruitt & Krauel (2010).

Inspection of the data that accompany Pruitt and Krauel's study of individual variation in satiation threshold and a comparison of these data with the Materials and Methods and Results sections of the paper have revealed a number of issues that cast doubts on the reliability of the data and any results based on these data. In particular, we show that, following our analyses, the data are unlikely to have been obtained using the study design outlined in the publication and that statistical analyses of these data provide results that differ in important ways from those reported. These findings illustrate the importance of making raw data and analysis code available for the rigour and reproducibility of the scientific literature.

Limited mass-independent individual variation in resting metabolic rate in a wild population of snow voles (Chionomys nivalis).

Resting metabolic rate (RMR) is a potentially important axis of physiological adaptation to the thermal environment. However, our understanding of the causes and consequences of individual variation in RMR in the wild is hampered by a lack of data, as well as analytical challenges. RMR measurements in the wild are generally characterized by large measurement errors and a strong dependency on mass. The latter is problematic when assessing the ability of RMR to evolve independently of mass. Mixed models provide a powerful and flexible tool to tackle these challenges, but they have rarely been used to estimate repeatability of mass-independent RMR from field data. We used respirometry to obtain repeated measurements of RMR in a long-term study population of snow voles (Chionomys nivalis) inhabiting an environment subject to large circadian and seasonal fluctuations in temperature. Using both uni- and bivariate mixed models, we quantify individual repeatability in RMR and decompose repeatability into mass-dependent and mass-independent components, while accounting for measurement error. RMR varies among individuals, that is, is repeatable (R = .46) and strongly co-varies with BM. Indeed, much of the repeatability of RMR is attributable to individual variation in BM, and the repeatability of mass-independent RMR is reduced by 41% to R = .27. These empirical results suggest that the evolutionary potential of RMR independent of mass may be severely constrained. This study illustrates how to leverage bivariate mixed models to model field data for metabolic traits, correct for measurement error and decompose the relative importance of mass-dependent and mass-independent physiological variation.

Bigger Is Fitter? Quantitative Genetic Decomposition of Selection Reveals an Adaptive Evolutionary Decline of Body Mass in a Wild Rodent Population.

In natural populations, quantitative trait dynamics often do not appear to follow evolutionary predictions. Despite abundant examples of natural selection acting on heritable traits, conclusive evidence for contemporary adaptive evolution remains rare for wild vertebrate populations, and phenotypic stasis seems to be the norm. This so-called "stasis paradox" highlights our inability to predict evolutionary change, which is especially concerning within the context of rapid anthropogenic environmental change. While the causes underlying the stasis paradox are hotly debated, comprehensive attempts aiming at a resolution are lacking. Here, we apply a quantitative genetic framework to individual-based long-term data for a wild rodent population and show that despite a positive association between body mass and fitness, there has been a genetic change towards lower body mass. The latter represents an adaptive response to viability selection favouring juveniles growing up to become relatively small adults, i.e., with a low potential adult mass, which presumably complete their development earlier. This selection is particularly strong towards the end of the snow-free season, and it has intensified in recent years, coinciding which a change in snowfall patterns. Importantly, neither the negative evolutionary change, nor the selective pressures that drive it, are apparent on the phenotypic level, where they are masked by phenotypic plasticity and a non causal (i.e., non genetic) positive association between body mass and fitness, respectively. Estimating selection at the genetic level enabled us to uncover adaptive evolution in action and to identify the corresponding phenotypic selective pressure. We thereby demonstrate that natural populations can show a rapid and adaptive evolutionary response to a novel selective pressure, and that explicitly (quantitative) genetic models are able to provide us with an understanding of the causes and consequences of selection that is superior to purely phenotypic estimates of selection and evolutionary change.

Heritable spouse effects increase evolutionary potential of human reproductive timing.

Sexual reproduction is inherently interactive, especially in animal species such as humans that exhibit extended pair bonding. Yet we have little knowledge of the role of male characteristics and their evolutionary impact on reproductive behavioural phenotypes, to the extent that biologists typically consider component traits (e.g. reproductive timing) as female-specific. Based on extensive genealogical data detailing the life histories of 6435 human mothers born across four centuries of modern history, we use an animal modelling approach to estimate the indirect genetic effect of men on the reproductive phenotype of their partners. These analyses show that a woman's reproductive timing (age at first birth) is influenced by her partner's genotype. This indirect genetic effect is positively correlated with the direct genetic effect expressed in women, such that total heritable variance in this trait is doubled when heritable partner effects are considered. Our study thus suggests that much of the heritable variation in women's reproductive timing is mediated via partner effects, and that the evolutionary potential of this trait is far greater than previously appreciated.

Humans as a model for understanding biological fundamentals.

How special are humans? This question drives scholarly output across both the sciences and the humanities. Whereas some disciplines, and the humanities in particular, aim at gaining a better understanding of humans per se, most biologists ultimately aim to understand life in general. This raises the question of whether and when humans are acceptable, or even desirable, models of biological fundamentals. Especially for basic biological processes, non-human species are generally accepted as a relevant model to study topics for which studying humans is impractical, impossible, or ethically inadvisable, but the reverse is controversial: are humans 'too unique' to be informative with respect to biological fundamentals relevant to other species? Or are there areas where we share key components, or for which our very uniqueness serves to allow novel explorations? In this special feature, authors from disciplines including biology, psychology, anthropology, neuroscience and philosophy tackle this question. Their overall conclusion is a qualified yes: humans do tell us about biological fundamentals, in some contexts. We hope this special feature will spur a discussion that will lead to a more careful delineation of the similarities and the differences between humans and other species, and how these impact the study of biological fundamentals.

Consistent cooperation in a cichlid fish is caused by maternal and developmental effects rather than heritable genetic variation.

Studies on the evolution of cooperative behaviour are typically confined to understanding its adaptive value. It is equally essential, however, to understand its potential to evolve, requiring knowledge about the phenotypic consistency and genetic basis of cooperative behaviour. While previous observational studies reported considerably high heritabilities of helping behaviour in cooperatively breeding vertebrates, experimental studies disentangling the relevant genetic and non-genetic components of cooperative behaviour are lacking. In a half-sibling breeding experiment, we investigated the repeatability and heritability of three major helping behaviours performed by subordinates of the cooperatively breeding fish Neolamprologus pulcher To experimentally manipulate the amount of help needed in a territory, we raised the fish in two environments differing in egg predation risk. All three helping behaviours were significantly repeatable, but had very low heritabilities. The high within-individual consistencies were predominantly due to maternal and permanent environment effects. The perceived egg predation risk had no effect on helping, but social interactions significantly influenced helping propensities. Our results reveal that developmentally plastic adjustments of provided help to social context shape cooperative phenotypes, whereas heritable genetic variation plays a minor role.

Pedigree-based inbreeding coefficient explains more variation in fitness than heterozygosity at 160 microsatellites in a wild bird population.

Although the pedigree-based inbreeding coefficient F predicts the expected proportion of an individual's genome that is identical-by-descent (IBD), heterozygosity at genetic markers captures Mendelian sampling variation and thereby provides an estimate of realized IBD. Realized IBD should hence explain more variation in fitness than their pedigree-based expectations, but how many markers are required to achieve this in practice remains poorly understood. We use extensive pedigree and life-history data from an island population of song sparrows (Melospiza melodia) to show that the number of genetic markers and pedigree depth affected the explanatory power of heterozygosity and F, respectively, but that heterozygosity measured at 160 microsatellites did not explain more variation in fitness than F This is in contrast with other studies that found heterozygosity based on far fewer markers to explain more variation in fitness than F Thus, the relative performance of marker- and pedigree-based estimates of IBD depends on the quality of the pedigree, the number, variability and location of the markers employed, and the species-specific recombination landscape, and expectations based on detailed and deep pedigrees remain valuable until we can routinely afford genotyping hundreds of phenotyped wild individuals of genetic non-model species for thousands of genetic markers.

Successful by Chance? The Power of Mixed Models and Neutral Simulations for the Detection of Individual Fixed Heterogeneity in Fitness Components.

Heterogeneity in fitness components consists of fixed heterogeneity due to latent differences fixed throughout life (e.g., genetic variation) and dynamic heterogeneity generated by stochastic variation. Their relative magnitude is crucial for evolutionary processes, as only the former may allow for adaptation. However, the importance of fixed heterogeneity in small populations has recently been questioned. Using neutral simulations (NS), several studies failed to detect fixed heterogeneity, thus challenging previous results from mixed models (MM). To understand the causes of this discrepancy, we estimate the statistical power and false positive rate of both methods and apply them to empirical data from a wild rodent population. While MM show high false-positive rates if confounding factors are not accounted for, they have high statistical power to detect real fixed heterogeneity. In contrast, NS are also subject to high false-positive rates but always have low power. Indeed, MM analyses of the rodent population data show significant fixed heterogeneity in reproductive success, whereas NS analyses do not. We suggest that fixed heterogeneity may be more common than is suggested by NS and that NS are useful only if more powerful methods are not applicable and if they are complemented by a power analysis.

Mother-offspring and nest-mate resemblance but no heritability in early-life telomere length in white-throated dippers.

Telomeres are protective DNA-protein complexes located at the ends of eukaryotic chromosomes, whose length has been shown to predict life-history parameters in various species. Although this suggests that telomere length is subject to natural selection, its evolutionary dynamics crucially depends on its heritability. Using pedigree data for a population of white-throated dippers (Cinclus cinclus), we test whether and how variation in early-life relative telomere length (RTL, measured as the number of telomeric repeats relative to a control gene using qPCR) is transmitted across generations. We disentangle the relative effects of genes and environment and test for sex-specific patterns of inheritance. There was strong and significant resemblance among offspring sharing the same nest and offspring of the same cohort. Furthermore, although offspring resemble their mother, and there is some indication for an effect of inbreeding, additive genetic variance and heritability are close to zero. We find no evidence for a role of either maternal imprinting or Z-linked inheritance in generating these patterns, suggesting they are due to non-genetic maternal and common environment effects instead. We conclude that in this wild bird population, environmental factors are the main drivers of variation in early-life RTL, which will severely bias estimates of heritability when not modelled explicitly.

Natural selection acts in opposite ways on correlated hormonal mediators of prenatal maternal effects in a wild bird population.

Maternal hormones are important mediators of prenatal maternal effects. Although many experimental studies have demonstrated their potency in shaping offspring phenotypes, we know remarkably little about their adaptive value. Using long-term data on a wild collared flycatcher (Ficedula albicollis) population, we show that natural selection acts in opposite ways on two maternally derived androgens, yolk androstenedione (A4) and yolk testosterone (T). High yolk A4 concentrations are associated with higher fitness, whereas high yolk T concentrations are associated with lower fitness. Natural selection thus favours females that produce eggs with high A4 and low T concentrations. Importantly, however, there exists a positive (non-genetic) correlation between A4 and T, which suggests that females are limited in their ability to reach this adaptive optimum. Thereby, these results provide strong evidence for an adaptive value of differential maternal androgen deposition, and a mechanistic explanation for the maintenance of variation in maternal investment in the wild.

A relationship between attractiveness and performance in professional cyclists.

Females often prefer to mate with high quality males, and one aspect of quality is physical performance. Although a preference for physically fitter males is therefore predicted, the relationship between attractiveness and performance has rarely been quantified. Here, I test for such a relationship in humans and ask whether variation in (endurance) performance is associated with variation in facial attractiveness within elite professional cyclists that finished the 2012 Tour de France. I show that riders that performed better were more attractive, and that this preference was strongest in women not using a hormonal contraceptive. Thereby, I show that, within this preselected but relatively homogeneous sample of the male population, facial attractiveness signals endurance performance. Provided that there is a relationship between performance-mediated attractiveness and reproductive success, this suggests that human endurance capacity has been subject to sexual selection in our evolutionary past.

The multivariate egg: quantifying within- and among-clutch correlations between maternally derived yolk immunoglobulins and yolk androgens using multivariate mixed models.

Egg components are important mediators of prenatal maternal effects in birds and other oviparous species. Because different egg components can have opposite effects on offspring phenotype, selection is expected to favour their mutual adjustment, resulting in a significant covariation between egg components within and/or among clutches. Here we tested for such correlations between maternally derived yolk immunoglobulins and yolk androgens in great tit (Parus major) eggs using a multivariate mixed-model approach. We found no association between yolk immunoglobulins and yolk androgens within clutches, indicating that within clutches the two egg components are deposited independently. Across clutches, however, there was a significant negative relationship between yolk immunoglobulins and yolk androgens, suggesting that selection has co-adjusted their deposition. Furthermore, an experimental manipulation of ectoparasite load affected patterns of covariance among egg components. Yolk immunoglobulins are known to play an important role in nestling immune defence shortly after hatching, whereas yolk androgens, although having growth-enhancing effects under many environmental conditions, can be immunosuppressive. We therefore speculate that variation in the risk of parasitism may play an important role in shaping optimal egg composition and may lead to the observed pattern of yolk immunoglobulin and yolk androgen deposition across clutches. More generally, our case study exemplifies how multivariate mixed-model methodology presents a flexible tool to not only quantify, but also test patterns of (co)variation across different organisational levels and environments, allowing for powerful hypothesis testing in ecophysiology.

Particle dispersion governs nano to bulk dynamics for tailored nanocomposite design.

Nanoparticle addition can expand bioplastic use, as the resultant nanocomposite features e.g., improved mechanical properties. HYPOTHESIS: It is generally hypothesised that the nanoparticle-polymer interaction strength is pivotal to reduce polymer dynamics within the interphasial region and beyond. EXPERIMENTS: Translating nanoscale phenomena to bulk properties is challenging, as traditional techniques that probe interphasial dynamics are limited to well-dispersed systems. Laser speckle imaging (LSI) enabled us to probe interphasial nanoscale dynamics of samples containing aggregated nanoparticles. We relate these LSI-derived relaxation times to bulk rheological properties at a micro scale. FINDINGS: Nanocomposites with well-dispersed PDMS-coated titanium dioxide nanoparticles of ∼100 nm showed higher viscosities than nanocomposites containing aggregated PVP- and PAA-coated nanoparticles of 200-2000 nm. Within the interphasial region, nanoparticle addition increased relaxation times by a factor 101-102, reaching ultraslow relaxations of ∼103 s. While the viscosity increased upon nanoparticle loading, interphasial relaxation times plateaued at 5 wt% for nanocomposites containing well-dispersed nanoparticles and 10 wt% for nanocomposites containing aggregated nanoparticles. Likely, interphasial regions between nanoparticles interact, which is more prominent in systems with well-dispersed nanoparticles and at higher loadings. Our results highlight that, contrary to general belief, nanoparticle dispersion seems of greater importance for mechanical reinforcement than the interaction between polymer and particle.

Low interspecific variation and no phylogenetic signal in additive genetic variance in wild bird and mammal populations.

Evolutionary adaptation through genetic change requires genetic variation and is a key mechanism enabling species to persist in changing environments. Although a substantial body of work has focused on understanding how and why additive genetic variance (V A) differs among traits within species, we still know little about how they vary among species. Here we make a first attempt at testing for interspecific variation in two complementary measures of V A and the role of phylogeny in shaping this variation. To this end, we performed a phylogenetic comparative analysis using 1822 narrow-sense heritability (h 2) for 68 species of birds and mammals and 378 coefficients of additive genetic variance (CV A) estimates for 23 species. Controlling for within-species variation attributable to estimation method and trait type, we found some interspecific variation in h 2 (~15%) but not CV A. Although suggestive of interspecific variation in the importance of non-(additive) genetic sources of variance, sample sizes were insufficient to test this hypothesis directly. Additionally, although power was low, no phylogenetic signal was detected for either measure. Hence, while this suggests interspecific variation in V A is probably small, our understanding of interspecific variation in the adaptive potential of wild vertebrate populations is currently hampered by data limitations, a scarcity of CV A estimates and a measure of their uncertainty in particular.

Rapid decline of prenatal maternal effects with age is independent of postnatal environment in a precocial bird.

Maternal effects are an important source of phenotypic variation with potentially large fitness consequences, but how their importance varies with the quality of the environment across an individual's ontogeny is poorly understood. We bred Japanese quail (Coturnix japonica) of known pedigree and experimentally manipulated the quality of the offspring diet, to estimate the importance of prenatal maternal effects in shaping variation in body mass from hatching to adulthood. Maternal genetic effects on body mass at hatching were strong, and largely caused by variation in egg mass, but their importance rapidly declined with age. Whereas there was a large effect of diet on growth, this did not affect the decline of maternal effects variance. The importance of additive genetic and residual variance increased with age, with the latter being considerably larger in the poor diet treatment. Hence, we found no evidence for prenatal maternal effect by postnatal environment interactions and that prenatal maternal effects are rapidly replaced by direct additive genetic and residual effects when offspring start to develop outside the egg. Thereby these results shed new light on the dynamics of the role of maternal versus offspring genes across ontogeny and environments.

When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring.

Quality differences between offspring sired by the social and by an extra-pair partner are usually assumed to have a genetic basis, reflecting genetic benefits of female extra-pair mate choice. In the zebra finch (Taeniopygia guttata), we identified a colour ornament that is under sexual selection and appears to have a heritable basis. Hence, by engaging in extra-pair copulations with highly ornamented males, females could, in theory, obtain genes for increased offspring attractiveness. Indeed, sons sired by extra-pair partners had larger ornaments, seemingly supporting the genetic benefit hypothesis. Yet, when comparing ornament size of the social and extra-pair partners, there was no difference. Hence, the observed differences most likely had an environmental basis, mediated, for example, via differential maternal investment of resources into the eggs fertilized by extra-pair and social partners. Such maternal effects may (at least partly) be mediated by egg size, which we found to be associated with mean ornament expression in sons. Our results are consistent with the idea that maternal effects can shape sexual selection by altering the genotype-phenotype relationship for ornamentation. They also caution against automatically attributing greater offspring attractiveness or viability to an extra-pair mate's superior genetic quality, as without controlling for differential maternal investment we may significantly overestimate the role of genetic benefits in the evolution of extra-pair mating behaviour.

Evolutionary genetics: evolution of mate choice in the wild.

Qvarnström et al. test whether the preference of female collared flycatchers (Ficedula albicollis) for males with large forehead patches could have evolved as a by-product of selection acting on male patch size. They find that the crucial genetic correlation between female choice and male patch size is not significant, and conclude that preference for large patches must have been shaped directly by selection. However, their use of the patch size of a female's social partner as a measure of choice is incomplete, and will result in low estimates of the potential for direct selection to shape female preference. Their study is therefore unable to resolve the question of how female preference for large forehead patches has evolved.

Low-coverage reduced representation sequencing reveals subtle within-island genetic structure in Aldabra giant tortoises.

Aldabrachelys gigantea (Aldabra giant tortoise) is one of only two giant tortoise species left in the world and survives as a single wild population of over 100,000 individuals on Aldabra Atoll, Seychelles. Despite this large current population size, the species faces an uncertain future because of its extremely restricted distribution range and high vulnerability to the projected consequences of climate change. Captive-bred A. gigantea are increasingly used in rewilding programs across the region, where they are introduced to replace extinct giant tortoises in an attempt to functionally resurrect degraded island ecosystems. However, there has been little consideration of the current levels of genetic variation and differentiation within and among the islands on Aldabra. As previous microsatellite studies were inconclusive, we combined low-coverage and double-digest restriction-associated DNA (ddRAD) sequencing to analyze samples from 33 tortoises (11 from each main island). Using 5426 variant sites within the tortoise genome, we detected patterns of within-island population structure, but no differentiation between the islands. These unexpected results highlight the importance of using genome-wide genetic markers to capture higher-resolution genetic structure to inform future management plans, even in a seemingly panmictic population. We show that low-coverage ddRAD sequencing provides an affordable alternative approach to conservation genomic projects of non-model species with large genomes.