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This study examined whether encoding conditions that encourage thoughts about the environment of evolutionary adaptation (EEA) are necessary to produce optimal recall in the adaptive memory paradigm. Participants were asked to judge a list of words for their relevance to personal survival under two survival-based scenarios. In one condition, the EEA-relevant context was specified (i.e., you are trying to survive on the savannah/grasslands). In the other condition, no context was specified (i.e., you are simply trying to stay alive). The two tasks produced virtually identical recall despite participants in the former condition reporting significantly more EEA context-relevant thoughts (i.e., the savannah) than did participants in the latter condition (who reported virtually no EEA-related thoughts). The findings are discussed in terms of (1) survival as a target of natural selection and (2) the role of evolutionary theory in understanding memory in modern humans.

Populations of the flour beetle Tribolium castaneum with histories of strong versus weak sexual selection purge mutation load and resist extinction differently. Mutational load minimized by sexual selection Sexual reproduction is more costly than the asexual kind because the genetic contribution of a given individual to the next generation is halved. A disadvantage of asexual reproduction is the accumulation of mutations, and it has been suggested that sexual selection, which acts when reproduction is achieved through competition and choice, might purge mutation. Matthew Gage and colleagues tested this theory in a study of populations of the flour beetle Tribolium castaneum raised for seven years under conditions of strong or weak sexual selection. Lineages from populations that had previously experienced strong sexual selection were resilient to extinction and maintained fitness, even with strong inbreeding, with some families continuing to survive after 20 generations of sibling–sibling mating. By contrast, lineages derived from populations that experienced weak or non-existent sexual selection showed rapid fitness declines under inbreeding, and all were extinct after the tenth generation. Reproduction through sex carries substantial costs, mainly because only half of sexual adults produce offspring 1 . It has been theorized that these costs could be countered if sex allows sexual selection to clear the universal fitness constraint of mutation load 2 , 3 , 4 . Under sexual selection, competition between (usually) males and mate choice by (usually) females create important intraspecific filters for reproductive success, so that only a subset of males gains paternity. If reproductive success under sexual selection is dependent on individual condition, which is contingent to mutation load, then sexually selected filtering through ‘genic capture’ 5 could offset the costs of sex because it provides genetic benefits to populations. Here we test this theory experimentally by comparing whether populations with histories of strong versus weak sexual selection purge mutation load and resist extinction differently. After evolving replicate populations of the flour beetle Tribolium castaneum for 6 to 7 years under conditions that differed solely in the strengths of sexual selection, we revealed mutation load using inbreeding. Lineages from populations that had previously experienced strong sexual selection were resilient to extinction and maintained fitness under inbreeding, with some families continuing to survive after 20 generations of sib × sib mating. By contrast, lineages derived from populations that experienced weak or non-existent sexual selection showed rapid fitness declines under inbreeding, and all were extinct after generation 10. Multiple mutations across the genome with individually small effects can be difficult to clear, yet sum to a significant fitness load; our findings reveal that sexual selection reduces this load, improving population viability in the face of genetic stress.

Manipulation of the frequency of naturally occurring colour patterns within replicate pools of fish at three sites shows that males with rare colour patterns have higher reproductive fitness, demonstrating negative frequency-dependent selection mediated by sexual selection. Reasons to be different Given that natural selection is both ubiquitous and remorseless, how is it that variation is maintained in populations? This pressing question in evolutionary biology is answered by Kimberly Hughes and colleagues in a study of guppies ( Poecilia reticulata ), a particularly useful model system because guppy male colouration is one of the most genetically variable organismal traits known. It was shown previously that in a population of brightly coloured guppies, males with rare colour patterns tend to thrive, against expectation. Hughes et al . show, using carefully controlled wild populations, not only that female guppies prefer to mate with these rare males, but that the males produce more offspring than those of more common stripe. This phenomenon, known as negative frequency-dependent selection, shows that there is a price on exclusivity and provides a mechanism for maintaining variation in a population. To understand the processes that maintain genetic diversity is a long-standing challenge in evolutionary biology, with implications for predicting disease resistance, response to environmental change, and population persistence 1 , 2 , 3 . Simple population genetic models are not sufficient to explain the high levels of genetic diversity sometimes observed in ecologically important traits 2 . In guppies ( Poecilia reticulata ), male colour pattern is both diverse and heritable, and is arguably one of the most extreme examples of morphological polymorphism known 4 , 5 . Negative frequency-dependent selection (NFDS), a form of selection in which genotypes are favoured when they are rare 6 , can potentially maintain such extensive polymorphism, but few experimental studies have confirmed its operation in nature 7 , 8 . Here we use highly replicated experimental manipulations of natural populations to show that males with rare colour patterns have higher reproductive fitness, demonstrating NFDS mediated by sexual selection. Rare males acquired more mates and sired more offspring compared to common males and, as previously reported, had higher rates of survival 8 . Orange colour, implicated in other studies of sexual selection in guppies, did predict male reproductive success, but only in one of three populations. These data support the hypothesis that NFDS maintains diversity in the colour patterns of male guppies through two selective agents, mates and predators. Similar field-based manipulations of genotype frequencies could provide a powerful approach to reveal the underlying ecological and behavioural mechanisms that maintain genetic and phenotypic diversity.

Understanding how natural selection has shaped genetic architecture of complex traits is of importance in medical and evolutionary genetics. Bayesian methods have been developed using individual-level GWAS data to estimate multiple genetic architecture parameters including selection signature. Here, we present a method (SBayesS) that only requires GWAS summary statistics. We analyse data for 155 complex traits (n = 27k–547k) and project the estimates onto those obtained from evolutionary simulations. We estimate that, on average across traits, about 1% of human genome sequence are mutational targets with a mean selection coefficient of ~0.001. Common diseases, on average, show a smaller number of mutational targets and have been under stronger selection, compared to other traits. SBayesS analyses incorporating functional annotations reveal that selection signatures vary across genomic regions, among which coding regions have the strongest selection signature and are enriched for both the number of associated variants and the magnitude of effect sizes. Methods to study how natural selection shapes genetic architecture of complex traits rely on individual level genome-wide association study (GWAS) data. Here, the authors present a Bayesian method using GWAS summary statistics to study genetic architecture and apply this to 155 complex traits.

Temporal variation in natural selection is predicted to strongly impact the evolution and demography of natural populations, with consequences for the rate of adaptation, evolution of plasticity, and extinction risk. Most of the theory underlying these predictions assumes a moving optimum phenotype, with predictions expressed in terms of the temporal variance and autocorrelation of this optimum. However, empirical studies seldom estimate patterns of fluctuations of an optimum phenotype, precluding further progress in connecting theory with observations. To bridge this gap, we assess the evidence for temporal variation in selection on breeding date by modeling a fitness function with a fluctuating optimum, across 39 populations of 21 wild animals, one of the largest compilations of long-term datasets with individual measurements of trait and fitness components. We find compelling evidence for fluctuations in the fitness function, causing temporal variation in the magnitude, but not the direction of selection. However, fluctuations of the optimum phenotype need not directly translate into variation in selection gradients, because their impact can be buffered by partial tracking of the optimum by the mean phenotype. Analyzing individuals that reproduce in consecutive years, we find that plastic changes track movements of the optimum phenotype across years, especially in bird species, reducing temporal variation in directional selection. This suggests that phenological plasticity has evolved to cope with fluctuations in the optimum, despite their currently modest contribution to variation in selection.

Understanding how microbial communities develop is essential for predicting and directing their future states. Ecological theory suggests that community development is often influenced by priority effects, in which the order and timing of species arrival determine how species affect one another. Priority effects can have long-lasting consequences, particularly if species arrival history varies during the early stage of community development, but their importance to the human gut microbiota and host health remains largely unknown. Here, we explore how priority effects might influence microbial communities in the gastrointestinal tract during early childhood and how the strength of priority effects can be estimated from the composition of the microbial species pool. We also discuss factors that alter microbial transmission, such as delivery mode, diet and parenting behaviours such as breastfeeding, which can influence the likelihood of priority effects. An improved knowledge of priority effects has the potential to inform microorganism-based therapies, such as prebiotics and probiotics, which are aimed at guiding the microbiota towards a healthy state.

Joel Hirschhorn and colleagues examine height-associated SNPs in northern- and southern-European populations. They report evidence of widespread weak selection on standing variation for height in humans. Strong signatures of positive selection at newly arising genetic variants are well documented in humans 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , but this form of selection may not be widespread in recent human evolution 9 . Because many human traits are highly polygenic and partly determined by common, ancient genetic variation, an alternative model for rapid genetic adaptation has been proposed: weak selection acting on many pre-existing (standing) genetic variants, or polygenic adaptation 10 , 11 , 12 . By studying height, a classic polygenic trait, we demonstrate the first human signature of widespread selection on standing variation. We show that frequencies of alleles associated with increased height, both at known loci and genome wide, are systematically elevated in Northern Europeans compared with Southern Europeans ( P < 4.3 × 10 −4 ). This pattern mirrors intra-European height differences and is not confounded by ancestry or other ascertainment biases. The systematic frequency differences are consistent with the presence of widespread weak selection (selection coefficients ∼10 −3 –10 −5 per allele) rather than genetic drift alone ( P < 10 −15 ).

Hong Xu and colleagues demonstrate reduced germline replication and selection against the transmission of mitochondria encoding a temperature-sensitive cytochrome c oxidase subunit. Although mitochondrial DNA (mtDNA) is prone to mutation and few mtDNA repair mechanisms exist 1 , crippling mitochondrial mutations are exceedingly rare 2 . Recent studies have demonstrated strong purifying selection in the mouse female germline 3 , 4 . However, the mechanisms underlying positive selection of healthy mitochondria remain to be elucidated. We visualized mtDNA replication during Drosophila melanogaster oogenesis, finding that mtDNA replication commenced before oocyte determination during the late germarium stage and was dependent on mitochondrial fitness. We isolated a temperature-sensitive lethal mtDNA allele, mt:CoI T300I , which resulted in reduced mtDNA replication in the germarium at the restrictive temperature. Additionally, the frequency of the mt:CoI T300I allele in heteroplasmic flies was decreased, both during oogenesis and over multiple generations, at the restrictive temperature. Furthermore, we determined that selection against mt:CoI T300I overlaps with the timing of selective replication of mtDNA in the germarium. These findings establish a previously uncharacterized developmental mechanism for the selective amplification of wild-type mtDNA, which may be evolutionarily conserved to limit the transmission of deleterious mutations.

Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications , to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species.

Changing environmental conditions cause changes in the distributions of phenotypic traits in natural populations. However, determining the mechanisms responsible for these changes-and, in particular, the relative contributions of phenotypic plasticity versus evolutionary responses-is difficult. To our knowledge, no study has yet reported evidence that evolutionary change underlies the most widely reported phenotypic response to climate change: the advancement of breeding times. In a wild population of red deer, average parturition date has advanced by nearly 2 weeks in 4 decades. Here, we quantify the contribution of plastic, demographic, and genetic components to this change. In particular, we quantify the role of direct phenotypic plasticity in response to increasing temperatures and the role of changes in the population structure. Importantly, we show that adaptive evolution likely played a role in the shift towards earlier parturition dates. The observed rate of evolution was consistent with a response to selection and was less likely to be due to genetic drift. Our study provides a rare example of observed rates of genetic change being consistent with theoretical predictions, although the consistency would not have been detected with a solely phenotypic analysis. It also provides, to our knowledge, the first evidence of both evolution and phenotypic plasticity contributing to advances in phenology in a changing climate.