The problem of the adaptive norm in human populations

The results of some investigations recently fulfilled in the framework of population-genetics approach to the problem of adaptive norm in human populations are summarized in this review. The main items considered are: methods of identification of morphologically "average" phenotypes, the role of stabilizing selection in maintaining the population adaptive norm, the problem of joint variation of monogenic and polygenic traits ant its relevance to "norm" and pathology. The significance of the concept of adaptive norm for preventive medicine and genetic monitoring is discussed.     

Bayesian variable selection for detecting adaptive genomic differences among populations

We extend an F(st)-based Bayesian hierarchical model, implemented via Markov chain Monte Carlo, for the detection of loci that might be subject to positive selection. This model divides the F(st)-influencing factors into locus-specific effects, population-specific effects, and effects that are specific for the locus in combination with the population. We introduce a Bayesian auxiliary variable for each locus effect to automatically select nonneutral locus effects. As a by-product, the efficiency of the original approach is improved by using a reparameterization of the model. The statistical power of the extended algorithm is assessed with simulated data sets from a Wright-Fisher model with migration. We find that the inclusion of model selection suggests a clear improvement in discrimination as measured by the area under the receiver operating characteristic (ROC) curve. Additionally, we illustrate and discuss the quality of the newly developed method on the basis of an allozyme data set of the fruit fly Drosophila melanogaster and a sequence data set of the wild tomato Solanum chilense. For data sets with small sample sizes, high mutation rates, and/or long sequences, however, methods based on nucleotide statistics should be preferred.     

Parallel adaptive divergence among geographically diverse human populations

Few genetic differences between human populations conform to the classic model of positive selection, in which a newly arisen mutation rapidly approaches fixation in one lineage, suggesting that adaptation more commonly occurs via moderate changes in standing variation at many loci. Detecting and characterizing this type of complex selection requires integrating individually ambiguous signatures across genomically and geographically extensive data. Here, we develop a novel approach to test the hypothesis that selection has favored modest divergence at particular loci multiple times in independent human populations. We find an excess of SNPs showing non-neutral parallel divergence, enriched for genic and nonsynonymous polymorphisms in genes encompassing diverse and often disease related functions. Repeated parallel evolution in the same direction suggests common selective pressures in disparate habitats. We test our method with extensive coalescent simulations and show that it is robust to a wide range of demographic events. Our results demonstrate phylogenetically orthogonal patterns of local adaptation caused by subtle shifts at many widespread polymorphisms that likely underlie substantial phenotypic diversity.     

The acute hypoxic ventilatory response: testing the adaptive significance in human populations

The acute Hypoxic Ventilatory Response (HVR) is an important component of human hypoxia tolerance, hence presumably physiological adaptation to high altitude. We measured the isocapnic HVR (L min(-1) %(-1)) in two genetically divergent low altitude southern African populations. The HVR does not differ between African Xhosas (X) and Caucasians (C) (X:-0.34+/-0.36; C:-0.42+/-0.33; P > 0.34), but breathing patterns do. Among all Xhosa subjects, size-independent tidal volume was smaller (X: 0.75+/-0.20; C: 1.11+/-0.32 L; P < 0.01), breathing frequency higher (X: 22.2+/-5.7; C: 14.3+/-4.2 breaths min(-1); P < 0.01) and hypoxic oxygen saturation lower than among Caucasians (X: 78.4+/-4.7%; C: 81.7+/-4.7%; P < 0.05). The results remained significant if subjects from Xhosa and Caucasian groups were matched for gender, body mass index and menstrual cycle phase in the case of females. The latter also employed distinct breathing patterns between populations in normoxia. High repeatability (intra-class correlation coefficient) of the HVR in both populations (0.77-0.87) demonstrates that one of the prerequisites for natural selection, consistent between-individual variation, is met. Finally, we explore possible relationships between inter-population genetic distances and HVR differences among Xhosa, European, Aymara Amerindians, Tibetan and Chinese populations. Inter-population differences in the HVR are not attributable to genetic distance (Mantel Z-test, P = 0.59). The results of this study add novel support for the hypothesis that differences in the HVR, should they be found between other human populations, may reflect adaptation to hypoxia rather than genetic divergence through time.     

The genetic and environmental basis of adaptive differences in shoaling behaviour among populations of Trinidadian guppies,Poecilia reticulata

The degree of plasticity an individual expresses when moving into a new environment is likely to influence the probability of colonization and potential for subsequent evolution. Yet few empirical examples exist where the ancestral and derived conditions suggest a role for plasticity in adaptive genetic divergence of populations. Here we explore the genetic and plastic components of shoaling behaviour in two pairs of populations of Poecilia reticulata (Trinidadian guppies). We contrast shoaling behaviour of guppies derived from high‐ and low‐predation populations from two separate drainages by measuring the shoaling response of second generation laboratory‐reared individuals in the presence and absence of predator induced alarm pheromones. We find persistent differences in mean shoaling cohesion that suggest a genetic basis; when measured under the same conditions high‐predation guppies form more cohesive shoals than low‐predation guppies. Both high and low‐predation guppies also exhibit plasticity in the response to alarm pheromones, by forming tighter, more cohesive shoals. These patterns suggest a conserved capacity for adaptive behavioural plasticity when moving between variable predation communities that are consistent with models of genetic accommodation.     

Identifying genes underlying skin pigmentation differences among human populations

Skin pigmentation is a human phenotype that varies greatly among human populations and it has long been speculated that this variation is adaptive. We therefore expect the genes that contribute to these large differences in phenotype to show large allele frequency differences among populations and to possibly harbor signatures of positive selection. To identify the loci that likely contribute to among-population human skin pigmentation differences, we measured allele frequency differentiation among Europeans, Chinese and Africans for 24 human pigmentation genes from 2 publicly available, large scale SNP data sets. Several skin pigmentation genes show unusually large allele frequency differences among these populations. To determine whether these allele frequency differences might be due to selection, we employed a within-population test based on long-range haplotype structure and identified several outliers that have not been previously identified as putatively adaptive. Most notably, we identify the DCT gene as a candidate for recent positive selection in the Chinese. Moreover, our analyses suggest that it is likely that different genes are responsible for the lighter skin pigmentation found in different non-African populations. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

The adaptive dynamics of altruism in spatially heterogeneous populations

Abstract.— We study the spatial adaptive dynamics of a continuous trait that measures individual investment in altruism. Our study is based on an ecological model of a spatially heterogeneous population from which we derive an appropriate measure of fitness. The analysis of this fitness measure uncovers three different selective processes controlling the evolution of altruism: the direct physiological cost, the indirect genetic benefits of cooperative interactions, and the indirect genetic costs of competition for space. In our model, habitat structure and a continuous life cycle makes the cost of competing for space with relatives negligible. Our study yields a classification of adaptive patterns of altruism according to the shape of the costs of altruism (with decelerating, linear, or accelerating dependence on the investment in altruism). The invasion of altruism occurs readily in species with accelerating costs, but large mutations are critical for altruism to evolve in selfish species with decelerating costs. Strict selfishness is maintained by natural selection only under very restricted conditions. In species with rapidly accelerating costs, adaptation leads to an evolutionarily stable rate of investment in altruism that decreases smoothly with the level of mobility. A rather different adaptive pattern emerges in species with slowly accelerating costs: high altruism evolves at low mobility, whereas a quasi-selfish state is promoted in more mobile species. The high adaptive level of altruism can be predicted solely from habitat connectedness and physiological parameters that characterize the pattern of cost. We also show that environmental changes that cause increased mobility in those highly altruistic species can beget selection-driven self-extinction, which may contribute to the rarity of social species.     

The problem of adaptive individual choice in cultural evolution

This paper tries to explain how individuals manage adaptive individual choice (i.e., the decision to acquire a fitter than average behavior or idea rapidly and tractably) in cultural evolution, despite the fact that acquiring fitness information is very difficult. I argue that the means of solving this problem suggested in the cultural evolution literature largely are various types of decision rules employing representations of fitness correlated properties or states of affairs. I argue that the problem of adaptive individual choice is best solved where some of these learning rule representations are socially transmitted and some are biologically transmitted.

The adaptive potential of plant populations in response to extreme climate events

The frequency and magnitude of extreme climate events are increasing with global change, yet we lack predictions and empirical evidence for the ability of wild populations to persist and adapt in response to these events. Here, we used Fisher's Fundamental Theorem of Natural Selection to evaluate the adaptive potential of Lasthenia fremontii, a herbaceous winter annual that is endemic to seasonally flooded wetlands in California, to alternative flooding regimes that occur during El Niño Southern Oscillation (ENSO) events. The results indicate that populations may exhibit greater adaptive potential in response to dry years than wet years, and that the relative performance of populations will change across climate scenarios. More generally, our findings show that extreme climate events can substantially change the potential for populations to adapt to climate change by modulating the expression of standing genetic variation and mean fitness.     

A population-genetic perspective on the similarities and differences among worldwide human populations

Recent studies have produced a variety of advances in the investigation of genetic similarities and differences among human populations. Here, I pose a series of questions about human population-genetic similarities and differences, and I then answer these questions by numerical computation with a single shared population-genetic data set. The collection of answers obtained provides an introductory perspective for understanding key results on the features of worldwide human genetic variation.     

The social biology of human populations: Spontaneous group formation conforms to evolutionary predictions of adaptive aggregation patterns

Two experiments tested whether city commuter and pedestrian groups conformed with ecological predictions of adaptive group size, age, and sex composition. It was predicted that individuals with the greatest reproductive potential would optimize mating contacts and minimize competitive interference by segregating into small, mixed-sex groups, whereas more vulnerable individuals, too young or old for optimum fertility, would tend to aggregate independently of gender in larger groups, which may offer advantages for foraging and predator avoidance. To maximize reproductive potential, mature males should prefer grouping with young women of high fertility, whereas older women should prefer younger men. In Experiment 1, 2,432 persons in three cities were observed on buses, automobiles, and sidewalks, in yoked observations. As predicted, reproductively immature preschool and grade-school children formed larger groups than mature adults (p < 0.0001) and showed no sex differences in grouping. Elderly adults (with decreased reproductive potential) were also found in larger groups than younger adults (p < 0.01) and also showed no sex differences. Sexually mature men and women grouped more with the opposite sex than in all-male or all-female groups (p < 0.00001). Mature adult men were the least aggregative category (p < 0.01): they tended to be alone or in pairs with women, and all-male groups were conspicuously absent (p < 0.005). These findings were consistent across different socioeconomic levels, ethnicities, and subcultures in our samples (p = NS). In Experiment 2, 475 bus passengers in three cities were observed selecting seatmates in a naturalistic choice paradigm. Only sexually mature adults exhibited a significant preference for the sex of their seatmates (p < 0.0005): Young women chose most often to sit with other women, whereas young adult men more frequently chose seatmates of the opposite sex. Young women were chosen more often as seat partners than all age/sex categories combined (p < 0.0005). Young women chose older partners (p < 0.05), while middle-aged women preferred younger women and men (p < 0.0005) as companions. Results are explained in the context of canalized behaviors arising early in human evolution.     

The segregation of cancer-causing genes in human populations

Cancer can arise through genetic damage of a variety of sorts, including recessive and dominant mutations, large chromosomal rearrangements, and the inability of cells to repair damaged DNA. Many of these events can be studied by standard methods of genetic analysis and thereby furnish the means to localize the gene to a specific region in the human genome. However, conventional methods of segregation analysis cannot provide the molecular and cellular understanding of the process of gene action essential to informed intervention. Here, recent advances in molecular biology, immunology and biochemistry hold promise of providing the understanding of how normal cells control their replication and why cancer cells do not. Heretofore these techniques have been largely restricted to modest-sized studies, but the requisite assays have now reached a level of development that makes practicable large clinical and population-based studies. Collectively, through these rapidly evolving techniques, we may eventually achieve the acquisition of new methods of prevention, diagnosis and therapy, and a better awareness of the events that order the lives of our cells.     

Genetic variability of glutathione S-transferase enzymes in human populations: Functional inter-ethnic differences in detoxification systems

Glutathione S-Transferase enzymes (GSTs) constitute the principal Phase II superfamily which plays a key role in cellular detoxification and in other biological processes. Studies of GSTs have revealed that genetic polymorphisms are present in these enzymes and that some of these are Loss-of-Function (LoF) variants, which affect enzymatic functions and are related to different aspects of human health.     

On adaptive accuracy and precision in natural populations

Adaptation is usually conceived as the fit of a population mean to a fitness optimum. Natural selection, however, does not act only to optimize the population mean. Rather, selection normally acts on the fitness of individual organisms in the population. Furthermore, individual genotypes do not produce invariant phenotypes, and their fitness depends on how precisely they are able to realize their target phenotypes. For these reasons we suggest that it is better to conceptualize adaptation as accuracy rather than as optimality. The adaptive inaccuracy of a genotype can be measured as a function of the expected distance of its associated phenotype from a fitness optimum. The less the distance, the more accurate is the adaptation. Adaptive accuracy has two components: the deviance of the genotypically set target phenotype from the optimum and the precision with which this target phenotype can be realized. The second component, the adaptive precision, has rarely been quantified as such. We survey the literature to quantify how much of the phenotypic variation in wild populations is due to imprecise development. We find that this component is often substantial and highly variable across traits. We suggest that selection for improved precision may be important for many traits.     

Parallelism in adaptive radiations of experimental Escherichia coli populations

Adaptive radiations are major contributors to species diversity. Although the underlying mechanisms of adaptive radiations, specialization and trade‐offs, are relatively well understood, the tempo and repeatability of adaptive radiations remain elusive. Ecological specialization can occur through the expansion into novel niches or through partitioning of an existing niche. To test how the mode of resource specialization affects the tempo and repeatability of adaptive radiations, we selected replicate bacterial populations in environments that promoted the evolution of diversity either through niche expansion or through niche partitioning, and in a third low‐quality single‐resource environment, in which diversity was not expected to evolve. Colony size diversity evolved equally fast in environments that provided ecological opportunities regardless of the mode of resource specialization. In the low‐quality environments, diversity did not consistently evolve. We observed the largest fitness improvement in the low‐quality environment and the smallest the glucose‐limited environment. We did not observe a change in the rate of evolutionary change in either trait or environment, suggesting that the pool of beneficial mutations was not exhausted. Overall, the mode of resource specialization did not affect the tempo or repeatability of adaptive radiations. These results demonstrate the limitations of eco‐evolutionary feedbacks to affect evolutionary outcomes.