The role of variation and plasticity in parental care during the adaptive radiation of three‐spine sticklebacks

Phenotypic plasticity might influence evolutionary processes such as adaptive radiations. Plasticity in parental care might be especially effective in facilitating adaptive radiations if it allows populations to persist in novel environments. Here, we test the hypothesis that behavioral plasticity by parents in response to predation risk facilitated the adaptive radiation of three‐spine sticklebacks. We compared the behavior of fathers across multiple ancestral (marine) and derived (freshwater) stickleback populations that differ in time since establishment. We measured behavioral plasticity in fathers in response to a predator found only in freshwater environments, simulating conditions marine males experience when colonizing freshwater. The antipredator behavior of males from newly established freshwater populations was intermediate between marine populations and well‐established freshwater populations. In contrast to our predictions, on average, there was greater behavioral plasticity in derived freshwater populations than in ancestral marine populations. However, we found greater individual variation in behavioral reaction norms in marine populations compared to well‐established freshwater populations, with newly established freshwater populations intermediate. This suggests that standing variation in behavioral reaction norms within ancestral populations might provide different evolutionary trajectories, and illustrates how plasticity can contribute to adaptive radiations.     

Geographic variation in winter hardiness of a common agricultural pest,Leptinotarsa decemlineata,the Colorado potato beetle

Successful latitudinal expansions into temperate climates depend largely upon the evolution of novel adaptive traits or the presence of pre-adaptive or exapted mechanisms for survival in seasonal climates. Geographic comparisons of ancestral (pre-expansion) and derived (post-expansion) populations provide a useful framework for understanding the evolutionary conditions that facilitate geographic expansions. Using a common agricultural pest, the Colorado Potato Beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae) as a model, we conducted a regional comparison of cold hardiness and overwintering success among ancestral (southern Mexico) and derived (Vermont and Kansas, USA) L. decemlineata populations. In order to determine if ancestral and derived beetle populations vary physiologically for cold hardiness, we compared supercooling points (SCPs) of three geographic populations of L. decemlineata. We also tested if ancestral and derived beetle populations differed in their overwintering behavior and success by performing an overwintering field experiment. Ancestral and derived populations did not express different physiological responses (i.e. SCPs) to freezing temperatures. However, ancestral and derived populations responded differently to the onset of winter conditions and displayed dissimilar overwintering behaviors. The majority of ancestral beetles failed to initiate diapause and dug upward within experimental mesocosms. Differences in overwintering behavior also resulted in significant variation in overwintering success as derived populations displayed higher overwintering survivorship when compared with ancestral populations. Given our results, it is evident that research exploring the interaction of the ecological factors and evolutionary processes is necessary to fully realize the dynamics of biological invasions.     

Controversies in the evolutionary social sciences: a guide for the perplexed

It is 25 years since modern evolutionary ideas were first applied extensively to human behavior, jump-starting a field of study once known as 'sociobiology'. Over the years, distinct styles of evolutionary analysis have emerged within the social sciences. Although there is considerable complementarity between approaches that emphasize the study of psychological mechanisms and those that focus on adaptive fit to environments, there are also substantial theoretical and methodological differences. These differences have generated a recurrent debate that is now exacerbated by growing popular media attention to evolutionary human behavioral studies. Here, we provide a guide to current controversies surrounding evolutionary studies of human social behavior, emphasizing theoretical and methodological issues. We conclude that a greater use of formal models, measures of current fitness costs and benefits, and attention to adaptive tradeoffs, will enhance the power and reliability of evolutionary analyses of human social behavior.     

Wealth,fertility and adaptive behaviour in industrial populations

The lack of association between wealth and fertility in contemporary industrialized populations has often been used to question the value of an evolutionary perspective on human behaviour. Here, we first present the history of this debate, and the evolutionary explanations for why wealth and fertility (the number of children) are decoupled in modern industrial settings. We suggest that the nature of the relationship between wealth and fertility remains an open question because of the multi-faceted nature of wealth, and because existing cross-sectional studies are ambiguous with respect to how material wealth and fertility are linked. A literature review of longitudinal studies on wealth and fertility shows that the majority of these report positive effects of wealth, although levels of fertility seem to fall below those that would maximize fitness. We emphasize that reproductive decision-making reflects a complex interplay between individual and societal factors that resists simple evolutionary interpretation, and highlight the role of economic insecurity in fertility decisions. We conclude by discussing whether the wealth–fertility relationship can inform us about the adaptiveness of modern fertility behaviour, and argue against simplistic claims regarding maladaptive behaviour in humans.     

Rapid evolutionary adaptation to elevated salt concentrations in pathogenic freshwater bacteria Serratia marcescens

Rapid evolutionary adaptions to new and previously detrimental environmental conditions can increase the risk of invasion by novel pathogens. We tested this hypothesis with a 133‐day‐long evolutionary experiment studying the evolution of the pathogenic Serratia marcescens bacterium at salinity niche boundary and in fluctuating conditions. We found that S. marcescens evolved at harsh (80 g/L) and extreme (100 g/L) salt conditions had clearly improved salt tolerance than those evolved in the other three treatments (ancestral conditions, nonsaline conditions, and fluctuating salt conditions). Evolutionary theories suggest that fastest evolutionary changes could be observed in intermediate selection pressures. Therefore, we originally hypothesized that extreme conditions, such as our 100 g/L salinity treatment, could lead to slower adaptation due to low population sizes. However, no evolutionary differences were observed between populations evolved in harsh and extreme conditions. This suggests that in the study presented here, low population sizes did not prevent evolution in the long run. On the whole, the adaptive potential observed here could be important for the transition of pathogenic S. marcescens bacteria from human‐impacted freshwater environments, such as wastewater treatment plants, to marine habitats, where they are known to infect and kill corals (e.g., through white pox disease).     

Experimental social evolution with Myxococcus xanthus

Genetically-based social behaviors are subject to evolutionary change in response to natural selection. Numerous microbial systems provide not only the opportunity to understand the genetic mechanisms underlying specific social interactions, but also to observe evolutionary changes in sociality over short time periods. Here we summarize experiments in which behaviors of the social bacterium Myxococcus xanthus changed extensively during evolutionary adaptation to two relatively asocial laboratory environments. M. xanthus moves cooperatively, exhibits cooperative multicellular development upon starvation and also appears to prey cooperatively on other bacteria. Replicate populations of M. xanthus were evolved in both structured (agar plate) and unstructured (liquid) environments that contained abundant resources. The importance of social cooperation for evolutionary fitness in these habitats was limited by the absence of positive selection for starvation-induced spore production or predatory efficiency. Evolved populations showed major losses in all measured categories of social proficiency- motility, predation, fruiting ability, and sporulation. Moreover, several evolved genotypes were observed to exploit the social behavior of their ancestral parent when mixed together during the developmental process. These experiments that resulted in both socially defective and socially exploitative genotypes demonstrate the power of laboratory selection experiments for studying social evolution at the microbial level. Results from additional selection experiments that place positive selection pressure on social phenotypes can be integrated with direct study of natural populations to increase our understanding of principles that underlie the evolution of microbial social behavior. This revised version was published online in August 2006 with corrections to the Cover Date.     

Demographic studies enhance the understanding of evolutionarily (mal)adaptive behaviors and phenomena in humans: a review on fertility decline and an integrated model

Recently, statistical analyses of demographic datasets have come to play an important role for studies into the evolution of human life history. In the first part of this paper, I highlight fertility decline, an evolutionarily paradoxical phenomenon in terms of fitness maximization. Then, I conduct a literature review regarding the effects of socioeconomic status on the number of offspring, especially in modern developed, (post-)industrial, and low-fertility societies. Although a non-positive relationship between them has often been recognized as a general feature of fertility decline, there actually exists a great deal of variation. Based on the review, I discuss the association between socioeconomic success and reproductive success, and tackle an evolutionary question as to why people seek higher socioeconomic success that would not directly lead to higher reproductive success. It has been suggested that, in modern competitive environments, parents should set a higher value on their investment in children, and aim to have a smaller number of high-quality children. Also, parents would maintain higher socioeconomic status for themselves so as to provide high-levels of investment in their children. In the second part, I broadly consider seemingly evolutionarily (mal)adaptive outcomes besides fertility decline, including child abuse, menopause, and suicide. The integration of the major three approaches to human behavioral and psychological research (behavioral ecology, evolutionary psychology, and cultural evolution) could lead to a deeper understanding. I provide a model for the integrated approach. Rich empirical evidence accumulated in demographic studies, especially longitudinal and cross-cultural resources, can assist to develop a theoretical framework.     

Testing evolutionary hypotheses about human biological adaptation using cross-cultural comparison

Physiological data from a range of human populations living in different environments can provide valuable information for testing evolutionary hypotheses about human adaptation. By taking into account the effects of population history, phylogenetic comparative methods can help us determine whether variation results from selection due to particular environmental variables. These selective forces could even be due to cultural traits-which means that gene-culture co-evolution may be occurring. In this paper, we outline two examples of the use of these approaches to test adaptive hypotheses that explain global variation in two physiological traits: the first is lactose digestion capacity in adults, and the second is population sex-ratio at birth. We show that lower than average sex ratio at birth is associated with high fertility, and argue that global variation in sex ratio at birth has evolved as a response to the high physiological costs of producing boys in high fertility populations.     

Environmental change, phenotypic plasticity, and genetic compensation

When a species encounters novel environmental conditions, some phenotypic characters may develop differently than in the ancestral environment. Most environmental perturbations of development are likely to reduce fitness, and thus selection would usually be expected to favor genetic changes that restore the ancestral phenotype. I propose the term "genetic compensation" to refer to this form of adaptive evolution. Genetic compensation is a subset of genetic accommodation and the reverse of genetic assimilation. When genetic compensation has occurred along a spatial environmental gradient, the mean trait values of populations in different environments may be more similar in the field than when representatives of the same populations are raised in a common environment (i.e., countergradient variation). If compensation is complete, genetic divergence between populations may be cryptic, that is, not detectable in the field. Here I apply the concept of genetic compensation to three examples involving carotenoid-based sexual coloration and then use these and other examples to discuss the concept in a broader context. I show that genetic compensation may lead to a cryptic form of reproductive isolation between populations evolving in different environments, may explain some puzzling cases in which heritable traits exposed to strong directional selection fail to show the expected evolutionary response, and may complicate efforts to monitor populations for signs of environmental deterioration.     

An Australasian test of the recent African origin theory using the WLH-50 calvarium

This analysis investigates the ancestry of a single modern human specimen from Australia, WLH-50 (Thorne et al., in preparation; Webb, 1989). Evaluating its ancestry is important to our understanding of modern human origins in Australasia because the prevailing models of human origins make different predictions for the ancestry of this specimen, and others like it. Some authors believe in the validity of a complete replacement theory and propose that modern humans in Australasia descended solely from earlier modern human populations found in Late Pleistocene Africa and the Levant. These ancestral modern populations are believed to have completely replaced other archaic human populations, including the Ngandong hominids of Indonesia. According to this recent African origin theory, the archaic humans from Indonesia are classified as Homo erectus, a different evolutionary species that could not have contributed to the ancestry of modern Australasians. Therefore this theory of complete replacement makes clear predictions concerning the ancestry of the specimen WLH-50. We tested these predictions using two methods: a discriminant analysis of metric data for three samples that are potential ancestors of WLH-50 (Ngandong, Late Pleistocene Africans, Levant hominids from Skhul and Qafzeh) and a pairwise difference analysis of nonmetric data for individuals within these samples. The results of these procedures provide an unambiguous refutation of a model of complete replacement within this region, and indicate that the Ngandong hominids or a population like them may have contributed significantly to the ancestry of WLH-50. We therefore contend that Ngandong hominids should be classified within the evolutionary species, Homo sapiens. The Multiregional model of human evolution has the expectation that Australasian ancestry is in all three of the potentially ancestral groups and best explains modern Australasian origins.     

On the Accessibility of Adaptive Phenotypes of a Bacterial Metabolic Network

The mechanisms by which adaptive phenotypes spread within an evolving population after their emergence are understood fairly well. Much less is known about the factors that influence the evolutionary accessibility of such phenotypes, a pre-requisite for their emergence in a population. Here, we investigate the influence of environmental quality on the accessibility of adaptive phenotypes of Escherichia coli''s central metabolic network. We used an established flux-balance model of metabolism as the basis for a genotype-phenotype map (GPM). We quantified the effects of seven qualitatively different environments (corresponding to both carbohydrate and gluconeogenic metabolic substrates) on the structure of this GPM. We found that the GPM has a more rugged structure in qualitatively poorer environments, suggesting that adaptive phenotypes could be intrinsically less accessible in such environments. Nevertheless, on average ∼74% of the genotype can be altered by neutral drift, in the environment where the GPM is most rugged; this could allow evolving populations to circumvent such ruggedness. Furthermore, we found that the normalized mutual information (NMI) of genotype differences relative to phenotype differences, which measures the GPM''s capacity to transmit information about phenotype differences, is positively correlated with (simulation-based) estimates of the accessibility of adaptive phenotypes in different environments. These results are consistent with the predictions of a simple analytic theory that makes explicit the relationship between the NMI and the speed of adaptation. The results suggest an intuitive information-theoretic principle for evolutionary adaptation; adaptation could be faster in environments where the GPM has a greater capacity to transmit information about phenotype differences. More generally, our results provide insight into fundamental environment-specific differences in the accessibility of adaptive phenotypes, and they suggest opportunities for research at the interface between information theory and evolutionary biology.     

Rapid climate change and the rate of adaptation: insight from experimental quantitative genetics

CONTENTS: Summary 752 I. Introduction 752 II. Will migration be enough? 753 III. Can adaptation proceed fast enough? 754 IV. Fitness links demographic and evolutionary processes 755 V. Experimental studies: what do they tell us and how can we improve them? 756 VI. Predicting evolutionary change based on genetic variation and natural selection 757 VII. The chronosequence approach 758 VIII. Resurrection of ancestral propagules 759 IX. The mean and variance in fitness, a link between genetics and demography 760 X. Conclusions 762 Acknowledgements 762 References 762 SUMMARY: Evolution proceeds unceasingly in all biological populations. It is clear that climate-driven evolution has molded plants in deep time and within extant populations. However, it is less certain whether adaptive evolution can proceed sufficiently rapidly to maintain the fitness and demographic stability of populations subjected to exceptionally rapid contemporary climate change. Here, we consider this question, drawing on current evidence on the rate of plant range shifts and the potential for an adaptive evolutionary response. We emphasize advances in understanding based on theoretical studies that model interacting evolutionary processes, and we provide an overview of quantitative genetic approaches that can parameterize these models to provide more meaningful predictions of the dynamic interplay between genetics, demography and evolution. We outline further research that can clarify both the adaptive potential of plant populations as climate continues to change and the role played by ongoing adaptation in their persistence.     

The Reproductive Ecology of Industrial Societies,Part II

Studies of the association between wealth and fertility in industrial populations have a rich history in the evolutionary literature, and they have been used to argue both for and against a behavioral ecological approach to explaining human variability. We consider that there are strong arguments in favor of measuring fertility (and proxies thereof) in industrial populations, not least because of the wide availability of large-scale secondary databases. Such data sources bring challenges as well as advantages, however. The purpose of this article is to illustrate these by examining the association between wealth and reproductive success in the United States, using the National Longitudinal Study of Youth 1979. We conduct a broad-based exploratory analysis of the relationship between wealth and fertility, employing both cross-sectional and longitudinal approaches, and multiple measures of both wealth (income and net worth) and fertility (lifetime reproductive success and transitions to first, second and third births). We highlight the kinds of decisions that have to be made regarding sample selection, along with the selection and construction of explanatory variables and control measures. Based on our analyses, we find a positive effect of both income and net worth on fertility for men, which is more pronounced for white men and for transitions to first and second births. Income tends to have a negative effect on fertility for women, while net worth is more likely to positively predict fertility. Different reproductive strategies among different groups within the same population highlight the complexity of the reproductive ecology of industrial societies. These results differ in a number of respects from other analyses using the same database. We suggest this reflects the impossibility of producing a definitive analysis, rather than a failure to identify the “correct” analytical strategy. Finally, we discuss how these findings inform us about (mal)adaptive decision-making.     

Rapid adaptation to a novel host in a seed beetle (Callosobruchus maculatus): the role of sexual selection

Rapid diversification is common among herbivorous insects and is often the result of host shifts, leading to the exploitation of novel food sources. This, in turn, is associated with adaptive evolution of female oviposition behavior and larval feeding biology. Although natural selection is the typical driver of such adaptation, the role of sexual selection is less clear. In theory, sexual selection can either accelerate or impede adaptation. To assess the independent effects of natural and sexual selection on the rate of adaptation, we performed a laboratory natural selection experiment in a herbivorous bruchid beetle (Callosobruchus maculatus). We established replicated selection lines where we varied natural (food type) and sexual (mating system) selection in a 2 x 2 orthogonal design, and propagated our lines for 35 generations. In half of the lines, we induced a host shift whereas the other half was kept on the ancestral host. We experimentally enforced monogamy in half of the lines, whereas the other half remained polygamous. The beetles rapidly adapted to the novel host, which primarily involved increased host acceptance by females and an accelerated rate of larval development. We also found that our mating system treatment affected the rate of adaptation, but that this effect was contingent upon food type. As beetles adapted to the novel host, sexual selection reinforced natural selection whereas populations residing close to their adaptive peak (i.e., those using their ancestral host) exhibited higher fitness in the absence of sexual selection. We discuss our findings in light of current sexual selection theory and suggest that the net evolutionary effect of reproductive competition may critically depend on natural selection. Sexual selection may commonly accelerate adaptation under directional natural selection whereas sexual selection, and the associated load brought by sexual conflict, may tend to depress population fitness under stabilizing natural selection.     

Were neandertal and modern human cranial differences produced by natural selection or genetic drift?

Most evolutionary explanations for cranial differences between Neandertals and modern humans emphasize adaptation by natural selection. Features of the crania of Neandertals could be adaptations to the glacial climate of Pleistocene Europe or to the high mechanical strains produced by habitually using the front teeth as tools, while those of modern humans could be adaptations for articulate speech production. A few researchers have proposed non-adaptive explanations. These stress that isolation between Neandertal and modern human populations would have lead to cranial diversification by genetic drift (chance changes in the frequencies of alleles at genetic loci contributing to variation in cranial morphology). Here we use a variety of statistical tests founded on explicit predictions from quantitative- and population-genetic theory to show that genetic drift can explain cranial differences between Neandertals and modern humans. These tests are based on thirty-seven standard cranial measurements from a sample of 2524 modern humans from 30 populations and 20 Neandertal fossils. As a further test, we compare our results for modern human cranial measurements with those for a genetic dataset consisting of 377 microsatellites typed for a sample of 1056 modern humans from 52 populations. We conclude that rather than requiring special adaptive accounts, Neandertal and modern human crania may simply represent two outcomes from a vast space of random evolutionary possibilities.     

Evolution of Stress-Regulated Gene Expression in Duplicate Genes of Arabidopsis thaliana

Due to the selection pressure imposed by highly variable environmental conditions, stress sensing and regulatory response mechanisms in plants are expected to evolve rapidly. One potential source of innovation in plant stress response mechanisms is gene duplication. In this study, we examined the evolution of stress-regulated gene expression among duplicated genes in the model plant Arabidopsis thaliana. Key to this analysis was reconstructing the putative ancestral stress regulation pattern. By comparing the expression patterns of duplicated genes with the patterns of their ancestors, duplicated genes likely lost and gained stress responses at a rapid rate initially, but the rate is close to zero when the synonymous substitution rate (a proxy for time) is >~0.8. When considering duplicated gene pairs, we found that partitioning of putative ancestral stress responses occurred more frequently compared to cases of parallel retention and loss. Furthermore, the pattern of stress response partitioning was extremely asymmetric. An analysis of putative cis-acting DNA regulatory elements in the promoters of the duplicated stress-regulated genes indicated that the asymmetric partitioning of ancestral stress responses are likely due, at least in part, to differential loss of DNA regulatory elements; the duplicated genes losing most of their stress responses were those that had lost more of the putative cis-acting elements. Finally, duplicate genes that lost most or all of the ancestral responses are more likely to have gained responses to other stresses. Therefore, the retention of duplicates that inherit few or no functions seems to be coupled to neofunctionalization. Taken together, our findings provide new insight into the patterns of evolutionary changes in gene stress responses after duplication and lay the foundation for testing the adaptive significance of stress regulatory changes under highly variable biotic and abiotic environments.     

Fitness recovery and compensatory evolution in natural mutant lines of C. elegans

Deleterious mutation accumulation plays a central role in evolutionary genetics, conservation biology, human health, and evolutionary medicine (e.g., methods of viral attenuation for live vaccines). It is therefore important to understand whether and how quickly populations with accumulated deleterious mutational loads can recover fitness through adaptive evolution. We used laboratory experimental evolution with four long-term mutation-accumulation (MA) lines of Caenorhabditis elegans nematodes to study the dynamics of such fitness evolution. We previously showed that when homozygous mutant populations are evolved in large population sizes, they can rapidly achieve wild-type fitness through the accumulation of new beneficial or compensatory epistatic mutations. Here, we expand this approach to demonstrate that when replicate lineages are initiated from the same mutant genotype, phenotypic evolution is only sometimes repeatable. MA genotypes that recovered ancestral fitness in the previous experiment did not always do so here. Further, the pattern of adaptive evolution in independently evolved replicates was contingent upon the MA genotype and varied among fitness-related traits. Our findings suggest that new beneficial mutations can drive rapid fitness evolution, but that the adaptive process is rendered somewhat unpredictable by its susceptibility to chance events and sensitivity to the evolutionary history of the starting population.     

Microgeographical diversification of threespine stickleback: body shape–habitat correlations in a small, ecologically diverse Alaskan drainage

Adaptive radiations are a major source of evolutionary diversity in nature, and understanding how they originate and how organisms diversify during the early stages of adaptive radiation is a major problem in evolutionary biology. The relationship between habitat type and body shape variation was investigated in a postglacial radiation of threespine stickleback in the upper Fish Creek drainage of Cook Inlet, Alaska. Although small, the upper Fish Creek drainage includes ecologically diverse lakes and streams in close proximity to one another that harbour abundant stickleback. Specimens from ancestral anadromous and derived resident freshwater populations differed substantially and could be distinguished by body shape alone, suggesting that the initial stages of adaptation contribute disproportionately to evolutionary divergence. Body shape divergence among resident freshwater populations was also considerable, and phenotypic distances among samples from freshwater populations were associated with habitat type but not geographical distance. As expected, stream stickleback from slow-moving, structurally complex environments tended to have the deepest bodies, stickleback from lakes with a mostly benthic habitat were similar but less extreme, and stickleback from lakes with a mostly limnetic habitat were the most shallow-bodied, elongate fish. Beyond adapting rapidly to conditions in freshwater environments, stickleback can diversify rapidly over small geographical scales in freshwater systems despite opportunities for gene flow. This study highlights the importance of ecological heterogeneity over small geographical scales for evolutionary diversification during the early stages of adaptive radiation, and lays the foundation for future research on this ecologically diverse, postglacial system.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 139–151.     

An evolutionary framework for common diseases: the ancestral-susceptibility model

Unlike rare mendelian diseases, which are due to new mutations (i.e. derived alleles), several alleles that increase the risk to common diseases are ancestral. Moreover, population genetics studies suggest that some derived alleles that protect against common diseases became advantageous recently. These observations can be explained within an evolutionary framework in which ancestral alleles reflect ancient adaptations to the lifestyle of ancient human populations, whereas the derived alleles were deleterious. However, with the shift in environment and lifestyle, the ancestral alleles now increase the risk of common diseases in modern populations. In this article, we develop an explicit evolutionary model and use population genetics simulations to investigate the expected haplotype structure and type of disease-association signals of ancestral risk alleles.